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Indicator and Methods For The Ecological Status Assessment Under The WFD Linkages Between Chemical and Biological Quality of Surface Waters
Indicator and Methods For The Ecological Status Assessment Under The WFD Linkages Between Chemical and Biological Quality of Surface Waters
EUROPEAN COMMISSION
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Indicators and methods for the ecological status assessment under the Water Framework Directive
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Preface
The Water Framework Directive (WFD; 2000/60/EC) creates a new legislative
framework to manage, use, protect, and restore surface water and groundwater
resources within river basins and transitional (lagoons and estuaries) and coastal
waters in the European Union. The WFD aims to achieve sustainable management
of water resources, to reach good ecological quality and prevent further deterioration
of surface waters and groundwater, and to ensure sustainable functioning of
aquatic ecosystems by 2015. In the WFD the ecological status of surface water is
dened as an expression of the quality of the structure and functioning of aquatic
ecosystems associated with surface waters, classied in accordance with Annex V
(Article 2:21). This implies that the classication systems of the ecological status
of water bodies should reect changes in the structure of the biological communities
and in the overall ecosystem functioning as a response to anthropogenic pressures.
Such requirements are a novel development in European water policy, which has
been mostly based on the regulation of emissions at the source through the
establishment of emission limit values.
The WFD necessitates that the ecological quality status of surface water bodies is
assessed using biological quality elements such as phytoplankton, sh, and benthic
ora and fauna. Therefore, there is a need to identify biological indicators that
respond in a predictable manner to human disturbances, and allow classication
of ecological quality based on functional relationships between pressures and
indicators. Currently, intensive research is being carried out in Europe to develop
biological indicators and classication metrics that can be used in assessment,
comparison and harmonization of ecological water quality targets across Europe.
This work is naturally based on the strong research tradition and knowledge on the
ecological functioning of surface waters in Europe. Still the WFD has imposed
challenges for aquatic ecologists to develop scientically sound, high-precision,
and practical biological assessment tools for managers.
This book provides an overview on current knowledge and methods on the
relationship between chemical and biological indicators for the major pressures for
rivers, lakes and coastal waters. It is aimed at scientists working in environmental
agencies, managers working on WFD implementation, university lecturers, students
of applied ecology, water management and those interested in limnology and
coastal management. Each section is dedicated to one of the major pressure types:
eutrophication, organic loading, acidication, toxic, and combined pressures which
IV |
PREFACE
are currently most widely impacting surface waters in Europe. An overview on the
known relationships between the pressure type in question and the biological
responses is provided for different surface water categories (rivers, lakes, coastal
and transitional waters). We have compiled information on the applicability of the
current existing biological classication tools and metrics, as well as the empirical
and deterministic models which include biological quality elements as parameters,
and could be used for WFD classication and management purposes. Finally, we
also provide information on some new emerging approaches and methodologies
that could be applied in the future.
This book is a deliverable of the EU FP6 REBECCA1 (Relationships between
ecological and chemical status of surface waters) project. The general objective of
the REBECCA project is to provide scientic support for the implementation of the
WFD. The two specic aims of the project are, rstly, to establish links between
ecological status of surface waters and physico-chemical quality elements and
pressures from different sources, and, secondly, to develop and validate tools that
member states can use in the process of classication, in the design of their
monitoring programs, and in the design of measures in accordance with the
requirements of the WFD.
We thank the Advisory Board of the REBECCA project (Ursula Schmedtje, Roger
Owen, Ivan Karottki, Joachim DEugenio, and Jorge Rodriguez-Romero) for constructive
comments and guidance on the contents and structure of this review. We are grateful
for a number of anonymous reviewers that provided suggestions for improvements.
We also wish to thank Gary Free for revising the language and providing comments
on a number of contributions. The opinions expressed in this book are those of the
authors, who are responsible for the contents of each chapter.
July 11, 2005, Ispra, Italy
The editors,
Angelo G. Solimini,
Ana Cristina Cardoso,
Anna-Stiina Heiskanen
REBECCA project is jointly funded by the EC 6th Framework programme as a Specic Targeted
Research or Innovation Project (Contract number SSPI-CT-2003-502158) and the research programmes
of the collaborating organizations. More information about REBECCA is available through the project
web-site at http://www.environment./syke/rebecca.
1
Contents
Contributors .............................................................................................................................
VII
33
81
99
Acidication
5. Acidication in rivers and lakes ................................................................................ 117
Torleif Bkken, Frode Kroglund, Eli-Anne Lindstrm, and Laurence Carvalho
Hydromorphological pressures
6. Hydromorophological pressures in lakes ................................................................ 135
Seppo Hellsten, Bernard Dudley
Toxic pressures
8. Impacts of selected hazardous and priority substances (WFD)
on freshwater and marine biota................................................................................ 151
Lena Blom and Eva Brorstrm-Lundn
VI |
CONTENTS
Combined pressures
11. Large scale evaluations of pressures........................................................................ 213
Ana Garcia, Bertrand Villeneuve, and Jean-Gabriel Wasson
Contributors
Contributors
Andersen, Jens Mller. National Environmental
Research Institute (NERI), Vejlsvej 25 DK 8600
Silkeborg, Denmark
VIII |
CONTRIBUTORS
Eutrophication and
organic pollution
1.1 Introduction
Within Europe, eutrophication has had a high prole since the early 1980s when wide-spread
occurrence of blue-green algal blooms in standing and slow-owing freshwaters gave rise to
considerable interest and concern by the public, the media and by water industries. Of all surface
waters, the impact of nutrient enrichment on lakes and reservoirs has probably received the
greatest attention and is well understood in general qualitative terms. Nutrients tend to be a
secondary and indirect driver of community composition but are a signicant driver of productivity,
leading to increased growths of algae (phytoplankton and lamentous algae) and aquatic plants.
The increase in phytoplankton crops can lead to secondary problems, such as the loss of sensitive
macrophyte and sh species. These impacts, as well as the increasing frequency and intensity of
toxic cyanobacteria blooms, have become a widespread problem in European lakes and have
considerable consequent environmental, social and economic implications.
These general effects of increased nutrient loading, or eutrophication, have been incorporated
within the denition of eutrophication in recent European legislation - Urban Waste Water
Treatment Directive (UWWTD) and Nitrates Directive (ND) and agreements (Oslo - Paris Marine
Convention, OSPAR). These dene eutrophication as:
The enrichment of water by nutrients, especially compounds of phosphorus (P) and/or nitrogen
(N), causing an accelerated growth of algae and higher forms of plant life to produce an undesirable
disturbance to the balance of organisms present in the water and to the quality of the water
concerned
One problem with this denition of eutrophication is that it cannot easily be quantied.
Eutrophication is a process, not a state such as eutrophic, the latter being more readily dened
in terms of phytoplankton biomass (e.g. as a concentration of chlorophyll-a) or a concentration of
a nutrient such as P. In the WFD, this issue of how to assess the degree of change in freshwater
quality is tackled by relating (ecological) quality to a baseline or reference state under minimal
human inuence. The requirement within the WFD to dene nutrient conditions for high and
good ecological status requires a specic quantitative dose-response understanding of how
nutrient conditions relate to biological quality in individual lake ecotypes.
The impact of nutrient pressures in a particular lake ecotype or individual site can be dependent
on a number of sensitivity factors. Deep lakes are often more predictable in terms of nutrient
effects on phytoplankton abundance and the indirect impacts on profundal (deep-water)
invertebrate and sh communities. In shallow lakes, ecological thresholds in response to nutrient
conditions are much more difcult to dene due to the feedback effects of macrophytes and sh
4 |
1.2 Phytoplankton
Introduction
The phytoplankton community is widely considered the rst biological community to respond to
eutrophication pressures and is the most direct indicator of all the Biological Quality Elements
(BQEs) of nutrient concentrations in the water column. There are numerous socio-economic
problems associated with increases in phytoplankton abundance, particularly with increasing
frequencies and intensities of toxic cyanobacteria blooms. These include detrimental effects on
drinking water quality, ltration costs for water supply (industrial and domestic), water-based
activities and conservation status (e.g. sensitive pelagic sh species, such as coregonids). In some
contexts, however, increasing phytoplankton abundance can be considered as a positive feature,
for example, in increasing sheries productivity, and some phytoplankton taxa can be considered
indicative of high ecological status.
Annex V of the WFD outlines three features of the phytoplankton quality element that need to be
considered in the assessment of the ecological status of lakes and for which there is thus the need
to relate in quantitative terms to nutrient conditions, i.e. for which dose-response curves need to
be investigated. These three are:
Phytoplankton composition
Phytoplankton abundance and its effect on transparency conditions
Planktonic bloom frequency and intensity.
The WFD normative denition indicates that declining ecological quality is associated with
increasing phytoplankton abundance, greater proportions of cyanobacteria and more frequent
and intense phytoplankton blooms. These three features are considered further in the context of
their specic use as metrics of nutrient pressures.
Phytoplankton composition
Individual species or taxa can be considered as positive, negative or indifferent indicators in
relation to nutrient pressures. Negative indicators include species of green algae (e.g. Scenedesmus)
and diatoms (e.g. Stephanodiscus) and many groups of cyanobacteria, such as the large colonial
and lamentous genera Microcystis, Aphanizomenon and Anabaena. The latter are favoured by
relatively stable stratication and high alkalinity and can, therefore, form a signicant natural
component of the phytoplankton community in deep alkaline lakes. As nutrient concentrations
increase, however, the dominance and abundance of cyanobacteria, in particular, generally
increases often resulting in dense, mono-specic blooms during summer (Reynolds, 1984).
The proportion of cyanobacteria of the total phytoplankton biomass is a metric that is being
recommended in Norway with regard to WFD requirements and for which thresholds can be
generated (Figure 1.1; Lyche Solheim et al., 2004). Positive indicators include species of chrysophytes
(e.g. Dinobryon), desmids (e.g. Cosmarium) and some diatoms (e.g. Cyclotella comensis).
The ratio of positive to negative species can be used as a metric of ecological status and some Member
States (Denmark - Sondergaard et al., 2003; UK Carvalho et al., 2004) are developing metrics based
on the relative abundance of positive and negative phytoplankton functional groups (as outlined in
Reynolds et al., 2002), rather than taxonomic units. Both taxonomic (Figure 1.1) and functional group
(Figure 1.2) dose-response relationships need to be developed and validated further.
1
Fraction cyano*
soft, clear
hard, clear
0.8
0.8
0.6
0.6
0.4
0.4
0.2
0.2
0
0.1
10
0.1
10
1
soft, humic
Fraction cyano*
hard, humic
0.8
0.8
0.6
0.6
0.4
0.4
0.2
0.2
0
0.1
1
10
Total phytoplankton biomass (mg WW / L)
0.1
1
10
Total phytoplankton biomass (mg WW / L)
6 |
10000
1000
100
10
1
0.1
1
10
TP (g l1)
100
1000
Figure 1.2 Relationship between biomass of the impact phytoplankton functional group Lm
(c.f. Reynolds et al., 2002) and total phosphorus concentrations in Finnish lakes (courtesy by Lepist et al.,
unpublished).
(a lake or more specically discrete points in a lake) while remote sensing methods can cover a
larger area at once (up to hundreds of lakes). A Secchi disk is a circular, 20 cm diameter, black and
white disk. The Secchi depth is the average of the depths where the disk disappears when lowered
into water and reappears again when raised. The actual photosynthetic layer of water is
approximately three times the Secchi disk depth. The Secchi disk method is a very simple, useful
and cost-effective way to monitor and assess the status of surface waters. Furthermore, this
method is a useful tool for monitoring by citizens to enhance public participation in the WFD. The
use of satellite remote sensing is, however, a cost-effective method to assess the transparency of
surface waters (turbidity, chlorophyll-a) on a large scale.
Quantitative relationships have been developed relating total phosphorus (TP) concentrations
with phytoplankton biomass (chlorophyll-a) and water clarity (Secchi depth). The most widely
reported relationships are those developed by Dillon and Rigler (1974) and Vollenweider OECD
(OECD, 1982). The latter relationship (Figure 1.3) was developed for a set of, predominantly large,
temperate lakes, not ecotype specic. There is a great deal of scatter in all the published
relationships highlighting the fact that a number of sensitivity factors are involved, such as water
colour and ushing rate, of which the latter can be altered by hydromorphological pressures such
as ow regulation. There is, therefore, a clear need to develop more complex regression models
that incorporate these sensitivity factors. The importance of such sensitivity factors highlights the
need to incorporate lake typology factors (e.g. depth, altitude, colour) into models to understand
how nutrients are transformed into algal biomass, highlighting the value of lake-type specic
models as advocated by the WFD.
[Chl] mg m3
10
} excluded
from regression
0.1
1
10
100
[P] mg m3
1000
8 |
Classication schemes
The most widely used classication scheme is that developed by the OECD (1982), which is
summarised in Table 1.1. Many other regression models or classication schemes have been
published which incorporate relationships between nutrients (exclusively phosphorus) and
phytoplankton (usually abundance) and transparency, summarised in Table 1.2.
Table 1.1 Lake classication scheme based on trophic status (OECD, 1982).
Annual mean
Total P
(g.l-1)
Annual mean
Chlorophyll-a (g.l-1)
Annual maximum
Chlorophyll-a
(g.l-1)
Annual mean
Secchi depth (m)
Ultra-oligotrophic
<4
<1
<2.5
>12
Oligotrophic
Mesotrophic
Eutrophic
Hyper-eutrophic
<10
10-35
35-100
>100
<2.5
2.5-8
8-25
>25
<8
8-25
25-75
>75
>6
6-3
3-1.5
<1.5
Models
Models simulating the impact of nutrients on the phytoplankton community can be divided into
three main categories:
1. Empirical statistical models
2. Mechanistic/deterministic models
3. Theoretical food-web models.
Many empirical statistical models have been developed based on correlations and regressions of
observed data on nutrient and chlorophyll-a concentrations and Secchi disc depth. Only one
published model relates Secchi depth to phytoplankton biomass (Hillbricht-Illkowska, 1993).
Caneld and Hodgson (1983), besides chlorophyll and Secchi disk depth, included dissolved
organic matter concentration to account for water colour in their model.
Region
Notes
Europe
Denmark
UK
Norway
The nutrient used in the published regressions is almost exclusively in-lake total phosphorus
concentration and the regressions are usually based on logarithmic transformations (Carlson,
1977; OECD, 1982; Mazumder and Haves, 1998; Portielje and van der Molen, 1999), only one is
based on a power function (Sas, 1989). In-lake TP concentrations can also be estimated using
data on lake depth, area, ushing rate and external TP loads using equations of Dillon and Rigler
(1974) and Kirchner and Dillon (1975). By linking the two, it is therefore possible to model how
changes in ushing rate and catchment land-use could affect phytoplankton abundance.
Deep lakes tend to show a much more predictable response than shallow lakes; it is therefore
possible that a relatively precise empirical model could be derived for deep European lakes to
predict impacts of changing nutrient conditions.
Mechanistic models which explore relationships between the physico-chemical environment and
the phytoplankton community are potentially useful for identifying reference conditions or
evaluating the effectiveness of restoration measures. A number of mechanistic models have been
10
developed which predict phytoplankton abundance and composition (DBS Model: PC Lake: Janse
and Van Liere, 1995; Los et al., 1997; Reynolds, 1999; PROTECH model: Elliott et al., 2001). Many
of these models incorporate mixing regimes and are capable of simulating multiple resource
limitation (phosphorus, nitrogen, etc.) and grazer effects.
Dynamic, deterministic models have also been developed to determine light attenuation in the
water column associated with phytoplankton (Kirk, 1994). Models such as CAEDYM, DYRESM,
SOBEK calculate light attenuation in the water column using Beers law with varying light
extinction coefcients for different algal groups, suspended sediments and dissolved organic
matter. From light attenuation, many models further calculate transparency. Theoretical models
examining lake ecosystem structure and functioning, in particular issues of stability and resistance
in shallow lakes, have been developed by Scheffer (1998).
1.3 Macrophytes
Introduction
The macrophyte community is generally regarded as a key indicator of the ecological status of
lakes as macrophytes provide habitat for many other aquatic biota (e.g. sh, macro-invertebrates,
wetland birds) to feed, seek refuge, or breed. Macrophytes are relatively long-lived organisms
(months to years), compared with phytoplankton and invertebrates. Macrophytes have a very
limited motility and are intrinsically linked to the prevailing environmental conditions in both the
surrounding lake water and sediments, through their roots and leaves. Individual species are
sensitive to physical and chemical changes in these media and hence are good indicators of both
current environmental conditions and longer-term environmental changes. Macrophytes, in terms
of assessing eutrophication pressure, can indicate enhanced nutrient concentrations through the
direct effects on species growth (biomass) and through indirect effects on species composition, as
may be caused by a reduction in transparency associated with nutrient-related increases in
phytoplankton and epiphyton.
Transparency is a key physico-chemical factor controlling the distribution and abundance of
submerged macrophytes in lakes. Changes occurring in the intensity and quality of light as it
passes down through the aquatic vegetation itself may exert a crucial effect on the development
and structure of aquatic macrophyte communities, as well as on the photosynthetic efciency and
productivity of the vegetation (Sculthorpe, 1967). Aquatic macrophytes are profoundly inuenced
by the transmission of light (the photosynthetically active radiation (PAR) through a water body,
which impacts upon photosynthetic processes. In turbid conditions the PAR passing through the
water can be attenuated by the scattering and absorption of light by suspended particles, both
organic and inorganic. Increasing turbidity can often result in a shift in community from submerged
to oating leaved or emergent species (Hough and Forwall, 1988). However, in terms of its impact
on aquatic macrophytes, turbidity can be difcult to separate from other properties of a lake, e.g.
colour and shading. Indeed, little is known of the precise inuence of underwater changes in light
intensity and quality on the distribution of life forms and species of aquatic macrophytes. It may
be that some plants of a particular habitat may tolerate, or even prefer sustained low intensities
and/or deciencies in certain wavelengths. Phenotypical variations due to abiotic circumstances
11
have been recorded for several species under changing inundation conditions e.g. Nabben et al.
1999; Van den Berg et al. 1999. Hyper-eutrophication may even lead to deterioration of emergent
and oating leaved communities due to reducing conditions in the sediment. These non-linear
responses of species composition and abundance to eutrophication pressures complicate the
indicator value of aquatic macrophytes.
Annex V of the WFD outlines two macrophyte-related quality elements that need consideration in
the assessment of the ecological status of lakes:
macrophyte community composition
macrophyte abundance.
Annex V of the WFD includes transparency as a physico-chemical element for supporting this
assessment of macrophyte communities. The WFD normative denitions for high, good and
moderate ecological status determine that ecological quality is considered as declining when the
composition of macrophytic taxa differ moderately from the type-specic communities and are
signicantly more distorted than those observed at good quality (slight changes in composition
and abundance of macrophytic taxa compared to the type-specic communities).
Metrics
The macrophyte community composition of lakes can be broadly related to a nutrient gradient, as
individual species appear to show differing tolerances to nutrient conditions, although research
suggests that other factors such as alkalinity, sediment type and water depth may be more
important in determining species composition (Penning, pers comm.). Some species such as Isoetes
lacustris, Potamogeton polygonifolius and Sparganium angustifolium tend to be restricted to low
alkalinity, oligotrophic lakes, other species, for example, Lemna spp, Myriophyllum spicatum and
Potamogeton pectinatus are typical of high alkalinity, (natural) eutrophic lakes. However, many
macrophyte species can be regarded as being indifferent to a change in trophic level, occurring
over a wider range of trophic conditions.
The relationship between the abundance of macrophytes and nutrients is complicated by internal
interactions between other ecological components of the ecosystem, particularly in shallow lakes
(Jeppesen et al., 2000; Moss et al., 2003). For example, Scheffer et al. (1993) produced an
alternative stable states model to describe shallow lake functioning. Rather than exhibiting
linear responses to changing nutrient concentrations, macrophyte species may undergo a threshold
response whereby they abruptly change from being abundant to a state where they are absent,
when phytoplankton dominate and vice versa. It appears that this can be due to initial spring
conditions, but also the characteristics of the sh community and management thereof can play
an important role (Van de Bund and Van Donk, 2002). Abundance can also be calculated as the
coverage of aquatic vegetation as a percentage of potential littoral area (USEPA, 1998;
Anonymous, 2003). Finnish case studies showed that helophytes and oating leaved vegetation
coverage could be related to an increase of phosphorus and nitrogen of lake water (Kanninen et al.,
2003; Leka et al., 2003). In shallow lakes macrophytes may even disappear when a hypereutrophic,
algal dominated state is reached (Blindow, 1992).
12 |
Although no comprehensive study has been undertaken to relate aquatic macrophytes with
turbidity/transparency measurements, a number of studies have examined the depth range of
individual species (e.g. Spence and Chrystal, 1970; Blindow, 1992; Wilby et al., 2000) or focused
on specic locations such as the Danube Delta, where Coops et al. (1999) classied lakes into
three different types that were related to turbidity ranges. In general, in relative terms, it appears
that the deeper a species grows, the less light the species requires and, therefore, the assumption
could be made that deeper growing species can compete better for light than other species and
will be more resistant to increased turbidity. However, not all species tolerant to low light and
growing at greater depths in clear lakes will successfully colonise lakes with high turbidity.
Exceptions may be species that are sensitive to factors such as eutrophication, substrate type,
siltation of leaves, or light quality, rather than just quantity of light (Davis and Brinson, 1980).
The sensitivity of North American submerged macrophytes to turbidity has been explored using the
Turbidity Tolerance Index, i.e. the ratio of the depth maxima of a species to the Secchi disc transparency
depth (Davis and Brinson, 1980). The Turbidity Tolerance Index provides an approximation of the
relative resilience of macrophyte species to turbidity stress and has been expanded to include more
species, including a number of which are known to occur in the UK (Adamus and Brandt, 1990). In
addition, species such as charophytes are thought to actively inuence the turbidity in their close
vicinity (Van den Berg et al., 1997; Van Donk and Van de Bund, 2002; Noges et al., 2003).
Classication schemes
In the Danube Delta Lakes project the lake typology in the Danube delta was described using
phytoplankton, hydrology, chemistry, macrophytes and sh species based on PCA analysis (Oosterberg
et al., 2000). Here, three groups of lakes could be characterised by their macrophyte communities by
correlating lakes with macrophytes and environmental factors, including nutrients. Coops et al.
(1999) also performed a classication for the Danube delta based on aquatic vegetation and
turbidity. For the WFD a number of macrophyte classication schemes have recently been reported
for Denmark (Sndergaard et al., 2003), the Netherlands (Van den Berg et al., unpublished), Finland
(Kanninen et al., 2003), Germany (Schaumberg et al., 2004), Northern Ireland (Dodkins et al., 2003)
and the UK (Willby, pers. comm.). All these macrophyte classication schemes share the common
characteristic of not being exclusively related to nutrients. Instead, most macrophyte classication
schemes are indirectly related to nutrient conditions. Examples are given in Table 1.3.
As no true direct relationship between transparency and macrophytes has been established, no
classication schemes for this parameter have been developed. Most classication schemes have
concentrated on the parameters that cause changes in transparency, and so are indirectly related.
In the case of nutrient pressures these have typically focused on the association of macrophyte
species with variables that correlate with trophic status (e.g. Palmer et al., 1992 - TRS and
alkalinity). The general expected trend in European lakes is that transparency will decrease with
increasing productivity of the water (Ellenberg, 1988; Palmer et al., 1992). The expected turbidity
states for various lake trophic types are as follows (see also Figure 1.4):
Dystrophic lakes coloured water
Oligotrophic (lime decient) lakes generally clear water
13
Table 1.3 Published examples of lake macrophyte models or classication schemes indirectly related to
nutrient conditions.
Reference
Region
UK
Notes
The Trophic Ranking Scheme (TRS) used the macrophyte composition recorded in
1224 standing waters to classify UK lakes into 10 vegetation groups, which were
related to lake alkalinity, pH and conductivity. Each of these 10 groups were
allocated site types based on lake trophy. Individual macrophyte species were also
allocated a TRS based on the range of site types within which they were found.
The average site TRS can be used to infer whether eutrophication has occurred.
However, the classication scheme is not reference based and does not directly
relate macrophyte species to nutrient conditions.
Sweden
The Swedish Environmental Quality Criteria (SEQC) scheme assesses the state of
lakes using a variety of factors including nutrients and species richness of
macrophytes. Comparisons of the current condition with reference values are used
in appraisals. The SEQC scheme denes conditions for both nutrient loadings and
macrophytes at high to low ecological status as well as deviations from the high
reference state. The macrophyte scheme is based on the UK TRS (Palmer et al.,
1992) and does not, however, directly relate the aquatic plant communities to
nutrient concentration data.
USA
The US EPA Lakes and Reservoir Bioassessment and Biocriteria uses submerged
macrophytes as one of 7 biological monitoring elements for assessing the condition
of US lakes. Lake condition is assessed using additive indices that integrate both
habitat and biological scores. The LRBB scheme provides reference values for
macrophyte metrics and nutrients but doesnt directly relate them together. This
multimetric index indicates the overall biological condition of a lake, however, it
cannot quantify the actual cause of degradation, although it does suggest where
eutrophication may be the cause.
Northern Ireland The Northern Ireland Lake Survey quantied macrophyte species environmental
relationships from over 500 lakes using Generalised Additive Models (GAM) and
Canonical Correspondence Analysis (CCA). Nutrient concentrations appeared
inuential in explaining species distribution, but were highly correlated with
alkalinity and altitude.
Romania
A classication of Danube Delta lakes based on aquatic macrophytes and
Europe
Preliminary macrophyte classication schemes developed specically for WFD.
Denmark
Finland
Germany
Northern Ireland
US EPA (1998)
turbidity.
14
10
Hypertrophic
Eutrophic
Oligotrophic Ultra-Oligotrophic
Mesotrophic
5
Av. yearly
Secchi disc
Transparency
0
5
1 15 2
10 15 20 30 50 m
Models
Detailed modelling studies have been carried out examining macrophyte attributes in relation to
environmental factors (e.g. Rrslett, 1991; Scheffer et al., 1993; Weisner et al., 1997; Muhammetoglu
and Soyupak, 2000; Aseada et al., 2001; Murphy, 2002; Murphy and Hootsmans, 2002). Linear
regression models and Generalised Additive Models have been employed to try and model the
response of individual macrophyte species to environmental conditions (Heegaard et al., 2001;
Van den Berg et al., 2003), or the interaction between species (Van Nes, 2002). These models
may have relevance for WFD bioassessment in linking macrophyte community attributes to
nutrient conditions.
However, as yet, no reliable quantitative models relating transparency and lake macrophyte
composition have been developed. However, it should be noted that in the Netherlands Schaminee
et al. (1995) described the vegetation types in the aquatic environment and included the main
abiotic characteristics. Bal et al. (1995) also provided detailed information of species composition
in relation to abiotic conditions. These paved the way for the development for the Dutch WFD
macrophyte classication scheme.
1.4 Phytobenthos
Introduction
Phytobenthos are an important component of primary production in lakes, although its contribution
to overall primary production decreases with increasing lake depth. In deep lakes, the phytobenthos
is, however, still an important component of littoral food webs, and will inuence the structure of
littoral macrophyte, invertebrate and sh communities. For example, an increasing abundance of
epiphyton, in response to nutrient enrichment, has long been considered an important factor in the
loss of submerged macrophytes (Phillips et al., 1978; Sand-Jensen and Sndergaard, 1981) and the
phytobenthos itself constitutes a signicant source of energy for most littoral invertebrate grazers.
15
Despite its potential signicance, phytobenthos has received relatively little attention in terms of
its use as an indicator of lake quality. The fact, that phytobenthos respond to both water column
nutrient concentrations and habitat quality, is accessible from the lake shore, and is less dynamic
than the phytoplankton community has led to increasing interest in its use as a monitoring tool
for lakes (US EPA, 1998).
Annex V of the Water Framework Directive specically outlines phytobenthos composition and
abundance as two criteria that need dening for type-specic ecological assessment of lakes in
relation to undisturbed conditions. Eutrophication of the overlying water generally results in an
enhanced growth of attached algae and changes in community composition. Species associated
with low phosphorus (the diatoms Achnanthidium minutissimum and Gomphonema tenellum)
and low nitrogen (nitrogen-xing species, such as the diatoms Epithemia adnata and Rhopalodia
gibba and cyanobacteria such as Anabaena spp.) waters have been shown to disappear following
nutrient enrichment (Fairchild et al., 1985). If nutrient enrichment proceeds further, phytoplankton
can shade the phytobenthos, reducing abundance and shifting community composition to species
tolerant of low light levels. The detailed response of the phytobenthos to nutrient conditions is,
however, much more complex than for phytoplankton. Nutrients diffuse much more slowly into
attached communities, with strong gradients through boundary layers and the attached
community. For example, denitrication by bacteria within biolms can result in nitrogen limitation
of the phytobenthos irrespective of nutrient availability in the water column. Further difculties,
in relating water column nutrient concentrations to benthic algae, is that they can also obtain
nutrients from the substrates that they are attached to.
Phytobenthos abundance is generally measured as chlorophyll-a per unit area of substrate.
However, quantitative analysis of phytobenthos abundance is much more difcult than for
phytoplankton, due to problems in standardising sampling area and the greater proportion of
detrital material within phytobenthos communities.
Only recently have attempts been made to develop quantitative relationships between the
phytobenthos community and nutrient conditions. Danilov and Ekelund (2000) analysed epiphyton
and epilithon species diversity from seven Swedish lakes. They concluded that epiphyton diversity
showed little relationship with nutrient concentrations, but epilithon diversity was consistently related
and could be used as an indicator of nutrient status. King et al. (2000) examined distributions of 138
epilithic diatom species from 17 lakes in the English Lake District and showed that total phosphorus
and calcium concentrations were the most important variables explaining species distributions.
16 |
Surface sediment diatom assemblages are important members of the phytobenthos community.
Direct, quantitative relationships between diatom species and total phosphorus concentrations
have been developed across Europe (Bennion, 1994; Wunsam and Schmidt, 1995). The combined
response of phytoplankton and phytobenthos communities is probably the most established
representation of lake ecosystem response to eutrophication and would be highly compatible with
palaeolimnological methods for the setting of reference conditions.
Models
No models have been established associating phytobenthos composition or abundance in lakes
to specic hydro-morphological or physico-chemical parameters.
17
Historically most studies have focused on the changes of the profundal benthic invertebrate
communities of deep stratifying lakes (mean depth greater than 3 m). In these deeper waters,
below the photic and wave action zones, environmental conditions tend to be relatively uniform
and predictable. In contrast, a greater variety of invertebrates are found in the more complex and
diverse habitat conditions of smaller shallow (mean depth less than 3 m), non-stratied lakes or
littoral areas of deep lakes.
The larvae of the midge genus Chironomus (chironomids belonging to the family Chironomidae)
are common in the profundal zones of lakes and reservoirs around the world (Armitage et al.,
1995). The capacity of these insects to live at very low oxygen concentrations is well known.
Chironomids are probably the most useful profundal indicator group for the trophic state of a
lake, as they have high species richness compared to other benthic invertebrate groups.
They occur over the whole spectrum of nutrient conditions and, because individual species have
highly specic environmental tolerances, they change species composition in tandem to changing
lake trophic status (Rosenberg, 1992). Multiple regression analyses of data from Spanish lakes
and reservoirs, showed that Chironomus density decreased with depth and temperature and
increased with alkalinity (Real, 2000).
Species indicative of eutrophic conditions will gradually colonize a lake (in most cases species
belonging to class Oligochaeta and family Chironomidae). Although, freshwater worms,
oligochaets (Oligochaeta) are more sensitive to changes in oxygen conditions than chironomids,
because they are less mobile and they feed and reproduce deeper in the sediments than the latter
(Lang, 1999).
Annex V of the WFD outlines the following benthic invertebrate quality components that need
consideration in the assessment of the ecological status of lakes:
Composition and abundance of benthic invertebrate fauna
Ratio of disturbance sensitive taxa to insensitive invertebrate taxa
Diversity of invertebrate communities.
In the WFD, a declining ecological quality is associated with poor diversity and dominance of a few
taxa. To comply with good ecological status the composition and abundance of invertebrate taxa, the
ratio of disturbance sensitive taxa to insensitive taxa and levels of diversity should show only slight
signs of alteration compared to the type-specic reference communities (Annex V, Section 1.2.2).
Metrics
Taxonomic composition. The tolerances of profundal macroinvertebrates to low dissolved oxygen
(DO) concentrations vary widely among species (Davis, 1975; Herreid, 1980). Attempts to devise
a lake typology for macroinvertebrates in general and specically for benthic chironomid
assemblages, based on trophic status and DO concentration, have met with varying degrees of
success (Brinkhurst, 1974), although clear general patterns exist. A combination of both sediment
type and oxygen supply have been shown to control the distribution of chironomids (Francis and
Kane, 1995) and oligochaetes (Verdonschot, 1996). The Orthocladiinae are characteristic of
highly oxygenated waters and thus tend to reect high status as does a high ratio of the
18 |
19
Classication schemes
Benthic invertebrates are widely utilised as indicators of organic pollution in freshwaters,
particularly rivers due to their sensitivity to oxygen conditions (Hynes, 1960; Hellawell, 1986).
Early classication schemes in lakes, similar to the Saprobic systems in rivers, were based mainly
on the analysis of the species composition of the chironomid communities. See Table 1.4 for
examples.
The Benthic Quality Index (BQI) was developed for assessing trophic status of Palearctic lakes
(Wiederholm, 1980). In these ecosystems, a eutrophic lakes BQI value is considered to be 1 and
Chironomus plumosus the dominant taxon; a BQI value of 5 is characteristic of an oligotrophic
lake. If no indicator species are present then a value of 0 is recorded and is indicative of a
hypereutrophic lake (Wiederholm, 1980). Lang developed three indices of trophy for lake Geneva
based on the structure of the Tubicidae and Lumbriculidae communities (Lang, 1998).
Numerous other studies highlight oxygen concentrations and food availability (as indicated by
total phosphorus, chlorophyll-a and algal biovolume) to be the most important communitystructuring factors linking chironomid communities with lake trophic state (e.g. Saether, 1979;
Brodin, 1982). In northern temperate waters these models have proved to be useful (e.g. Kansanen
et al., 1984) as long as oxygen concentrations in the profundal zone remained high enough to
support the chironomid communities (Brodersen and Lindegaard, 1999).
Table 1.4 Examples of benthic invertebrate classication systems and models.
Reference
Region
Wiederholm (1980)
Palearctic
Lang (1998)
Brodin (1982)
Heinis and Davids (1993)
Notes
Saether (1979)
Kansanen et al. (1984)
Lindegaard (1995)
Brodersen and Lindegaard (1999)
Dinsmore et al. (1999)
Alberta, Canada
Florida, USA
20 |
Models
Empirical models of profundal macroinvertebrate biomass using dissolved oxygen concentration
and water temperature as predictors have explained a signicant proportion of the variance
found in profundal macroinvertebrate biomass (PMB; Dinsmore et al., 1999). Residual variation
in this model is high suggesting that the model could be improved by obtaining more representative
estimates of PMB and water chemistry variables; including estimates of detrital production,
accumulation rate and composition; or by quantifying the effects of biotic factors such as
competition, predation, life history phenologies1, which have an important inuence on PMB in
habitats where dissolved oxygen and food materials are not limiting (Kajak, 1987).
Empirical models have established relationships between total phosphorus and the structure and
function of macroinvertebrate communities (e.g. King and Richardson, 2003). A model developed
for Lake Ladoga, North-Western Russia, reproduced the annual dynamics of zoobenthos biomass
and its distribution over the lake bed (Astrakhantsev et al., 2003).
1.6 Fish
Introduction
According to the cascading trophic interaction hypothesis a top predator such as piscivorous sh
can inuence the abundance, size-structure, and productivity of zooplankton and phytoplankton
(Carpenter and Kitchell, 1984; Carpenter et al., 1985). The bottom-up and top-down model
(McQueen et al., 1986; McQueen et al., 1989) combines the inuence of both predators (topdown) and resources (bottom-up). It predicts that top-down forces should be strong at the top of
the food web and weaken towards the bottom, whereas bottom-up forces should be strong at the
lower trophic level (algae) and weaken towards the top of the food chain (little or no inuence of
sh). Top- down pressure can exert substantial inuence on phytoplankton composition and
biomass through grazing pressure, however the importance depends on the number of food web
links (2 to 5) and trophic status of the lakes (oligo- to hyper-trophic).
Due to their complex ecological requirements, sh are sensitive indicators for habitat quality at
various spatial scales. As consumers and/or top predators, they integrate information on trophic
conditions across the food chain. They also provide detailed information on the respective trophic
level. There is a long tradition of linking the health of sh populations to water quality.
Dissolved oxygen is a dening and limiting parameter for sh, affecting survival, growth, spawning,
swimming performance, larval development and migration behaviour (Doudoroff and Shumway,
1970). Since oxygen is vital to other aquatic biota (i.e. invertebrates) that are a key food source
for sh, then the species composition and biomass of sh communities can also be affected
indirectly by oxygen availability. The composition of the sh community at a specic site is the
result of various factors including environmental factors such as temperature, oxygen, ow and
nutrients and the anthropogenic movement of sh.
1
Periodic life history events, such as breeding, migration, etc., which occur in relation to seasonality and climate.
21
Fish species can be separated by their oxygen requirements. As well as having different requirements
between species, they have different needs throughout their life stages (eggs, larvae, juveniles
and adults). Generally, stenotherms2 need higher oxygen concentrations than eurytherms3 and
adult sh tolerate low oxygen concentrations better than juveniles. The temperature of the
surrounding water has a substantial inuence on the dissolved oxygen concentration within the
water column, as well as signicantly affecting the physiological demand by sh. Warmer water
temperatures reduce the oxygen saturation capacity, as well as increasing the physiological
demand by the sh. The development of anoxia in lakes is most pronounced in thermally stratied
systems in summer and under the ice in winter when the water mass is cut-off from the atmosphere.
Besides the direct effects on aerobic organisms, anoxia can lead to increased release of phosphorus
from sediments that can fuel algal blooms when mixed into the upper euphotic (illuminated)
zone. It also leads to the build-up of chemically reduced compounds such as ammonium and
hydrogen sulphide (H2S) which can be toxic to bottom dwelling organisms. In extreme cases,
sudden mixing of H2S into the upper water column can cause sh kills.
The Water Framework Directive requires information on sh communities to be used in the
ecological quality assessment of lakes. Annex V of the WFD outlines three sh-related quality
elements that need consideration:
sh composition
sh abundance
sh age structure.
The WFD normative denitions of ecological status classication, indicate that: 1) changes in
species composition and abundance; 2) decreases in type sensitive species; and 3) changes in age
structure, as a sign of disturbance indicating a failure of reproduction or development of a
particular species; will downgrade water quality classication.
Classication schemes
Each sh species has characteristic requirements for water quality, habitat and environmental
conditions necessary to satisfy their need for breeding, feeding, growing, recruitment and survival.
These characteristics are used to classify sh species according to the concept of ecological/
functional guild, dened as a group of species that use the same class of environment conditions
in the same way (Root, 1967; Austen et al., 1994). Examples of classication schemes are
summarized in Table 1.5.
The European Fish-Index (EFI) developed by the FAME project4, is a multimetric sh-index for
classication of European rivers. The EFI is based on the same principle of the Index of Biotic
Integrity (IBI; Karr, 1981), where the fundamental assumption is that the composition and
structure of sh assemblages are impacted by human pressures in a predictable manner. In the
EFI the sh species were classied according to their zoogeographic status (Native, Introduced,
Organisms adapted** to only slight variations in temperature.
Organisms adapted*** to a wide range of temperature.
4
EVK1-CT-2001-00094; http://fame.boku.ac.at.
2
3
22 |
Region
Denmark
Notes
Nikolski (1962)
sensitivity.
Romania
Endemic), trophic guild, reproductive guild, habitat guild (degree of rheophily5 and habitat
preference in the water body), migratory behaviour, longevity and tolerance capacity (Schmutz et al.,
in prep.). Where possible, tolerance to specic stressors was assessed (temperature, acidication),
including habitat degradation and water quality. Where information was lacking an overall
assessment of general tolerance was made. A group of sentinel species, i.e. known to be common
in specic river-zones and providing good information on ecological quality, was identied for
5
23
each ecoregion. For these species, information regarding size or age structure is required in the
multimetric assessment. The EFI indicates the deviation from predicted reference metrics, and
provides a probability for a site to represent reference conditions.
Final ecological status of a site is identied by the degree of deviation from reference metrics. The
EFI is able to detect impacts of both physical and chemical pressures. However more precise data
on pressures are required to distinguish between different types of pressure. The EFI index cannot
be applied directly for sh biota in lakes, but the same approach could be applied to develop a
sh-index for lakes.
A Fish-based classication system has been developed for Danish lakes (Jeppesen et al., 2000).
Changes in sh species richness, biodiversity and trophic structure were linked to a trophic gradient
which was divided into ve total phosphorus (TP) classes (class 1-5: <0.05, 0.05-0.1, 0.1-0.2. 0.20.5, >0.4 mg P L-1). The sh species richness was unimodally related to TP, being highest at 0.1-0.4
mg P L-1. At low nutrient concentrations, piscivorous sh (particularly perch, Perca uviatilis) were
abundant and the biomass ratio of piscivores to plankti-benthivorous cyprinids was high and
density of cyprinids low. With increasing TP, a major shift in trophic structure occurred.
A classication system developed for 48 European lake ecotypes by the research project ECOFRAME
proposed 28 variables for water quality status from which three were sh parameters: sh
community, sh biomass and piscivorus-zooplanctivorus biomass ratio (Moss et al., 2003). The
advantages of the proposed classication system are that it applies variables that are inexpensive
to measure and ecologically relevant. The scheme was tested using data from 66 shallow lakes,
and may be adapted for more lakes after minor adjustments.
A classication of sh communities into lake ecology guilds, such as riverine/ white sh, eurytopic/
grey sh and limnophilic/ black sh has been proposed for Europe. White sh are Acipenseridae,
Salmonidae and Clupeidae, grey sh Percidae and Esocidae and black sh Umbridae and
Cobitidae; representatives of Cyprinidae turn up in all three classes (Regier et al., 1998). Except
for diadromous6 migratory species, all these categories are found in lakes of the Danube delta
that are connected to a river with a network of natural or man-made canals (Navodaru et al.,
2002). Abundance, biomass and species guild was used to describe a trophic gradient of Danube
delta lakes. PCA analysis was carried out to separate lake types for the Danube delta using
comprehensive data sets of hydrology, chemistry, vegetation, phytoplankton, and sh (Oosterberg
et al., 2000). Based on this study three types of lake were identied: Type I, mostly eutrophic with
intermediate sh species (grey and black), Type II, an intermediate with eurytopic/grey sh and
Type III, mesotrophic with limnophilic/black sh (Figure 1.5).
Models
Some examples of models for sh and environmental quality variables for lakes are reported in
Table 1.6. A study of 466 lakes from temperate to artic zones described the impact of nutrients
and lake depth on top-down control in the pelagic zone of lakes (Jeppesen et al., 2003). The study
6
24 |
1.0
1.0
(A)
(B)
Baclanesti
FilamAlg
ABRA BRAM
0.5
0.5
Cuibul cu lebede
Plin
CARA AURA
Furtuna
TINC TINC
RUTI RUTI
0.0
Serbata
ESOX LUCI
NitelObt
TravTim
Isac
CARA AURA
RUTI RUTI
Tataru
-0.5
AqVeget
CARA CARA
0.0
ESOX LUCI
-0.5
ALBU ALBU
BLIC BJOE
-0.5
0.0
Clay
Size
Reed
SCAR ERYT
Phyto
BLIC BJOE
PERC FLUV
PERC FLUV
-1.0
-1.0
Amplit
PotTrich ABRA BRAM
Organic
0.5
1.0
-1.0
-1.0
-0.5
0.0
0.5
1.0
Figure 1.5 PCA analysis of the relative biomass of 10 dominant sh species in 11 lakes in relation to trophic
variables, (A) species-site bi-plot of the rst two axes, and (B) species-environment bi-plot of the rst two axes.
Abbreviations of sh species are composed by the rst 4 letters of both genus and species names. Soil type
(ORGANIC, SAND or CLAY), morphometry (SIZE, DEPTH), hydrological distance (TRAVTIM) together with
subsequent residence time in the lake (CURESTM), water level uctuation (AMPLIT), chlorophyll a concentration
(PHYTO), lamentous algae (FILAMALG), aquatic vegetation coverage (AQVEGET), Potamogeton trichoides
(POTTRICH), Nitellopsis obtusa (NITELOBT) and reed: open water ratio (REED). (original from Navodaru et
al., 2002).
25
Table 1.6 Examples of models for sh and environmental quality variables for lakes.
Reference
Region
Notes
Denmark, Norway
Multiple regression model data from 466 lakes was used
(temperate, boreal and artic zones) to study impacts of lake trophic status on top-down control
by sh. The results indicated that planktivorous sh have a
more limited effect on the grazing control of phytoplankton
in oligotrophic lakes than in eutrophic lakes, despite similar
predator control of large-bodied zooplankton.
Hanson and Legged (1982)
Linear model for relationship between total phosphorus
Canada
(TP) and sh yield (Y) in two lakes:
LogY = 0.708 log TP + 0.774
Log Y = 0.072 TP + 0.792
Brmick and Lemcke (2003)
NW Germany
Data from 786 lakes was used to estimate sh yield
potential (FYP; kg.ha-1.a-1) for shallow and stratied lakes as
function of primary production of phytoplankton (PP) and
total phosphorus (TP)
lakes with PP<380: FYP= 6.315e0.0062.pp, r=0.47;
lakes with PP>380: FYP= 57.937 lnPP 278.09, r = 0.34
Northern
Finland
Study from an Artic lake Inari, indicated that an increase in
Lyytikainen and Jobling (1998)
lake temperature (T) resulted in an immediate increase in
oxygen consumption (M-accl in mg kg-1 h-1) tting to an
exponential model:
M-accl=46.53e(0.086T)
on these models, Brmik and Lemcke (2003) developed regional sh yield estimation models for
shallow and stratied lakes. The models take into account the ndings by Lang et al. (1981), who
state that the relation between PP and FYP changes from an exponential to a logarithmic function
with increasing PP values and approaches the upper asymptote. Accordingly, the following models
were obtained (Brmick and Lemcke, 2003):
FYP (for lakes with PP < 380): FYP(kg.ha-1.a-1) = 6.315e0.0062.pp, r = 0.47;
FPY (for lakes with PP > 380: FYP(kg.ha-1.a-1) = 57.937lnPP 278.09, r = 0.34
These models are capable of simulating the effects of a large variety of environmental conditions,
and can be used as dynamic tools for ecosystem risk assessment since they produce both qualitative
and quantitative results, allowing for comparisons of predictions with on-going observational
research and ecosystem monitoring.
1.7 Summary
Although the impact of nutrient pressures on biological quality is relatively well understood for
lakes in qualitative terms, there has been very limited development of quantitative dose-response
relationships, classication tools or models. This review identied a number of widely-recognised
strong relationships between physico-chemical measures of eutrophication and associated
biological responses. These can be split into two types of relationships: (1) primary responses
(phytoplankton, phytobenthos and macrophytes) to nutrient state, and (2), secondary responses
26 |
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33
2.1 Introduction
Coastal ecosystems receive anthropogenic nutrients from direct sources on the coastline or
indirectly from riverine export from catchments and from the atmosphere. Increasing and longterm nutrient loading from anthropogenic sources has caused eutrophication of coastal ecosystems,
the symptoms of which are: excess accumulation of phytoplankton biomass in the water column
and bottom sediments, depletion of oxygen in bottom waters, increased frequency of noxious
algal blooms, increased turbidity, deterioration of coastal food webs and reduction of biodiversity
(Figure 2.1).
At present, many coastal and estuarine ecosystems receive high rates of nutrient loading. Estimates
of the increase of phosphorus and nitrogen loading to estuarine systems range between 2-6-fold
and 1.5-14-fold compared to the turn of the 20th century (Conley, 1999; Cloern, 2001; Carstensen
et al., 2004). Atmospheric loading of nitrogen to the north Atlantic area has increased 5-10-fold
since industrialisation (Paerl and Whitall, 1999), and atmospheric deposition of nitrogen may
represent 10-50% of the anthropogenic N ux to water surfaces (Pryor and Barthelmie, 2000).
Nutrient loading from diffuse sources (e.g. arable and pastoral agricultural sources and forestry)
to the coastal waters is more difcult to estimate.
When considering eutrophication in coastal areas, of equal relevance as the concentrations of the
principal nutrients: nitrogen (N), phosphorus (P) and silicate (Si), are their ratios. As nitrate
concentrations increase due to anthropogenic loading, systems are moving towards not only
higher N:P ratios, but also lower Si:N ratios. As a consequence, coastal areas are likely to become
P and Si limited worldwide (Justic et al., 1995a,b), including northern Europe (Conley et al., 1993;
Jickells, 1998; Kristiansen and Hoell, 2002; Sommer et al., 2002; Turner et al., 2003).
In addition, other human activities such as damming of rivers leads to increased silicate retention
and less silicon export to the sea (Humborg et al., 2000a). During the last decades, N: P ratios
have increased dramatically in Dutch coastal waters (deJonge et al., 2002), Danish coastal areas
(Jorgensen, 1996; Kaas et al., 1996), and in the Black Sea (Shtereva et al., 1999).
Ecological indicators
Dale and Beyeler (2001) suggest a set of criteria that ecological indicators should meet when used
for assessing the condition of the environment. According to their criteria, the indicators should
be straightforward and relatively inexpensive to measure;
be sensitive to stresses of the system;
respond to stress in a predictable manner;
34
Transboundary
nutrient uxes
Nutrient input
N,P, Si
Increased concentrations of N, P, Si
N:P, N:Si ratios
Nuisance
algal
blooms
Macrophytobenthos biomass
and primary production
Increase in
phytoplankton
biomass
Increase in
primary production
Toxins
Increase in
turbidity
Decrease in
light regime
DIRECT EFFECTS
Oxygen
deciency
Increase
bacteria
35
both coastal and transitional waters, as well as sh for transitional waters only. In Tables 1.2.3.
and 1.2.4 of Annex V of the WFD, the normative denitions for high, good, and moderate status
are described in narrative terms. These tables provide more specic denitions on the quality
elements that should be used in the classication.
For the phytoplankton, the following quality elements need to be assessed:
Phytoplankton composition and abundance
Average phytoplankton biomass and water transparency
Frequency and intensity of phytoplankton blooms
According to the WFD, declining ecological quality of coastal and transitional waters is characterised
by a slight (good status) or moderate (moderate status) disturbance in the composition and
abundance of phytoplankton taxa, slight or moderate changes in the biomass, and slight or
moderate increases in the frequency and duration of phytoplankton blooms. Such disturbances are
evaluated against reference conditions set for each coastal or transitional water type.
For the macrophytes, the composition and abundance of macroalgae and angiosperms need to be
assessed. The WFD stipulates that at high ecological status all disturbance-sensitive macroalgal
and angiosperm taxa, which are normally associated with undisturbed conditions, must be present.
Also the levels of macroalgal cover and angiosperm abundance must be consistent with undisturbed
conditions. Similarly, to full good ecological status most disturbance-sensitive macroalgal and
angiosperm taxa associated with undisturbed conditions must be present and the levels of
macroalgal cover and angiosperm abundance must only show slight signs of disturbance.
Likewise, the composition and abundance of benthic invertebrate fauna needs to be assessed.
A decline in ecological quality is identied when the diversity of invertebrate taxa is outside the
range normally observed in high or reference conditions for each coastal type.
2.2 Phytoplankton
Phytoplankton biomass
Phytoplanktonic primary producers are the rst organisms to respond to elevated nutrient
concentrations in their environment. Most phytoplankton species, with the exception of
picoplanktonic algae, respond positively and predictably to nutrient enrichment in all European
coastal areas (Olsen et al., 2001). Phytoplankton react to increasing ambient nutrient availability
with increased growth i.e. primary production. Primary production is normally measured by the
incorporation of radioactively labelled carbon (14C) or by the O2 technique, and it normally shows
a rapid and positive response to nutrient increase (Smayda, 2004).
While primary production is directly linked to nutrient availability, biomass and composition of
phytoplankton are determined by the balance between growth and loss processes in the ecosystem.
The most important loss processes are food web interactions (grazing by zooplankton and benthic
animals) and hydrodynamic dispersion. The top-down control of phytoplankton and dispersion are
signicant determinants of the fate of nutrient input and subsequent phytoplankton growth in
coastal areas (Monbet, 1991; Kivi et al., 1993; Le Pape et al., 1996; Thomann and Linker, 1998;
36 |
Olsen et al., 2001; Perez-Ruzafa et al., 2002). Mussel beds on the bottom of estuaries can act as
a strong buffer against biomass accumulation, since the extra phytoplankton biomass is effectively
grazed by these lter-feeders (Le Pape and Menesguen, 1997; Meeuwig et al., 1998).
High phytoplankton biomass results in an increased amount of organic matter to be degraded by
bacteria and benthic fauna, which may lead to hypoxia or anoxia of bottom waters (Richardson
and Jrgensen, 1996). Long-lasting eutrophication may result in recurrent or even permanent
oxygen decit on bottoms, and collapse of bottom fauna. In anoxic conditions the nutrients that
have accumulated in sediments of estuaries and enclosed seas, such as the Baltic Sea, are released
again into the water column thus contributing further to eutrophication. However, the development
of hypoxia depends largely on hydrography in the area. Sheltered, non-tidal estuaries with
restricted water exchange are more vulnerable to oxygen deciency than tidal open estuaries,
where water exchange is substantial.
37
1.0
A
log (Chl (mgm-3))
log10 (Secchi, m)
0.9
0.8
0.7
0.6
0.5
0.4
1.2
y = -1.32x + 2.5
R2 = 0.89
1.3
1.4
log10TN mol l-1
1.5
1.6
2.4
2.6
2.8
3.0
3.2
Figure 2.2 Relationship between total nitrogen (TN) and (A) Secchi depth in Himmerfjrden, Baltic Sea
(Tett et al., 2003), and (B) Chlorophyll-a in small Finnish bayments, Baltic Sea (Meeuwig et al., 2000).
3.4
38 |
800
MesoMed
MesoBal
600
Lagoon
NorthSea
400
200
coordinated mesocosm studies revealed a signicantly lower biomass yield per unit nutrient
addition for coastal communities in the Mediterranean compared to Atlantic or Baltic (Figure 2.3).
The differences between the systems were attributed to differences in top-down control by
zooplankton, and vertical export (Olsen et al., 2001; Duarte, 2004).
39
economical. There are several long time-series of chlorophyll-a measurements available, although
differences in analytical procedures (mostly related to the extraction protocol), can hinder the
comparability of the results. A weak point in the use of total biomass or chlorophyll-a alone is that
these indicators hold virtually no information on phytoplankton community structure. A related
chemical approach: quantifying accessory algal pigments by HPLC, can provide information on
composition of communities (at group level) and still avoid the bias associated with microscopical
examination (Schlter et al., 2000).
Phytoplankton biomass shows considerable natural variability due to seasonal succession, tidal
mixing, and localised freshwater input. Therefore, the selection of time-windows from monitoring
data for analysis, as well as sampling frequency, can be crucial when using phytoplankton biomass
as an indicator (Johnson et al., 2000).
Transparency
Transparency is not specically mentioned as a quality element in the Water Framework Directive.
However, transparency is linked to normative denitions (WFD; Annex V, sections 1.2.3. and 1.2.4.)
of the phytoplankton quality element so that at high status phytoplankton should have a biomass
that does not signicantly alter the type specic transparency conditions. Therefore, transparency
is an important supporting element for assessing the ecological quality of a water body.
The transparency of the water column in coastal waters is an indirect result of nutrient loading
and nutrient status. Increased nutrient loading often increases phytoplankton biomass in the
water column, which in turn decreases the transparency. However, local discharges of suspended
solids, dissolved coloured substances, untreated sewage or industrial efuents, may directly affect
the transparency of the water. Low transparency conditions are also often found in large river
plumes and shallow tidal areas due to sediment resuspension.
Reduced transparency inhibits the penetration of light and decreases the depth of the euphotic
zone. As a consequence, there is insufcient light near the sediment for primary production, which
make the deep macrophyte populations (seagrasses and macroalgae) decline or disappear. Since
macrophyte species have different light demands, reduced transparency affects dominance
patterns of the vegetation as well. In addition, low transparency strongly decreases the recreational
value of coastal waters.
40 |
about 0.05 m y -1 (Sanden and Hkansson, 1996). Likewise, in the Adriatic water transparency has
decreased since, 1960 due to increased phytoplankton biomass related to nutrient enrichment via
the Po river discharge (Justic, 1988; Degobbis et al., 2000). In the Dutch Wadden Sea (the
Marsdiep) Cade and Hegeman (2002) found a decrease in the annual mean Secchi depth from
1.20 m to 1.0 m from the early, 1970s to 2000.
In some areas it has been possible to establish a quantitative relationship between transparency
and nutrient loading, either through direct correlation, or the use of more or less complex models.
For instance, in Danish estuaries, a signicant relationship has been established between total
nitrogen and chlorophyll-a concentration, as well as with Secchi depth (Nielsen et al., 2002a).
The use of transparency for assessing trophic status in coastal waters is not always straightforward
because inorganic suspended matter, detritus and humic substances can contribute more to
turbidity than phytoplankton (Wasmund et al., 2001). In such cases the transparency is not or
only weakly coupled to the nutrient loading or nutrient status of the system. In naturally turbid
waters such as some tidal areas, the anthropogenic discharges of nutrients may have little or no
effects on the transparency if, for example, the phytoplankton production is light limited and not
nutrient limited (Sanders et al., 2001; Colijn and Cade, 2003). Also in shallow non-stratied
areas the transparency can be more inuenced by the presence of a high density of suspension
feeding bottom fauna (e.g. mussels), than nutrient loading.
In near-shore Dutch waters the transparency was mostly determined by resuspended sediment,
while the contribution of phytoplankton to light extinction was of minor importance (van Gils and
Tatman, 2002; Blauw et al., 2004a,b). On the other hand, the variability in transparency in lake
Veerse Meer, a former tidal inlet that is now separated from the sea by dams, was 92% determined
by phytoplankton biomass (Stronkhorst et al., 1985). The underwater light climate in this deep
saltwater lake is strongly affected by the mixing layer depth following seasonal stratication.
Provided that the contribution from suspended solids is low and/or large data sets are at hand
the extinction coefcient may be distributed among the various phytoplankton groups using a
regression approach (van Gils and Tatman, 2002; Blauw et al., 2004a,b). On the other hand,
phytoplankters are inuenced differentially by light availability. Such effects may be quantied in
terms of PI-curves (production/irradiance) for different groups of phytoplankton or evaluated
based on observations of species composition along gradients of light availability (e.g. depth
distribution, correlation to suspended sediments).
41
One important factor in the response of phytoplankton species to nutrient enrichment is their
specic physiological characteristics, such as growth potential, nutrient afnity and capacity for
intracellular nutrient storage. Phytoplankton indicator species for eutrophication in coastal areas
have not yet been identied (Smayda, 2004). However, evidence suggests that invasive, colonistspecies, that have been recognised in anthropogenically disturbed water bodies are agellated,
small (high surface/volume ratio) and potentially form blooms, which are often toxic or otherwise
harmful (Sellner et al., 2001; Smayda and Reynolds, 2001). In contrast, it has also been found
that in eutrophic nitrogen-controlled environments large phytoplankton species dominate, whereas
the fraction of small-sized species increases towards oligotrophy (Kuosa, 1990; Jrgensen, 1996).
However, most toxic dinoagellate blooms occur along oligotrophic coasts in Europe, whereas
blooms of non-toxic Phaeocystis dominate in the eutrophicated southern North Sea.
Indicators for phytoplankton composition should ideally have the following requirements:
indicative and sensitive to eutrophication and nutrient loading pressures
widely applicable in European coastal areas
cost effective and easy to analyse
include key species or groups, which are important in production and fate of biomass
applicable for validation of ecosystem models.
Potential indicators
Diatoms/agellates shift of functional groups. Changes in ambient nutrient concentrations
and their ratios give a competitive advantage to some phytoplankton species over others (Ofcer
and Ryther, 1980; Egge and Aksnes, 1992). Silicate limitation, indicated by decreasing Si:N ratios
as a consequence of eutrophication may affect the phytoplankton community by decreasing the
relative biomass of diatoms and increasing the biomass of agellates, some of which may develop
into harmful algal blooms (Sommer, 1995; Escaravage et al., 1999).
It has been observed in the North Sea coastal area, that long-term eutrophication has not only led
to an increase in phytoplankton biomass (chlorophyll-a), but also changes in the phytoplankton
community structure with a shift towards larger diatoms, and Phaeocystis pouchetii (Haptophyta)
-dominated blooms (Philippart et al., 2000; Cade and Hegeman, 2002). A similar trend has been
found in the southern Baltic Sea (Wasmund and Uhlig, 2003), where long-term monitoring data
have showed a decline in diatoms and an increase in dinoagellates during the spring bloom.
Other factors that affect the relationship between anthropogenic nutrient loading and
phytoplankton abundance and composition include vertical mixing and underwater light climate.
When light is limiting phytoplankton growth, a change in nutrient loading is not likely to affect
phytoplankton growth. In turbid transitional waters with a tidal effect, benthic primary production
by microphytobenthos may account for a large part of local primary production. Also, vertical
mixing has a large inuence on the competition between agellates and diatoms. This effect is
usually not taken into account in experimental studies of competition between functional groups
of phytoplankton. Therefore the results of competition experiments do not necessarily match with
eld observations.
42 |
43
Diversity indices
Diversity indices1 have been developed to describe, quantify and simplify the species richness and
diversity of ecosystems. Their purpose is to combine information related to species abundance
and species richness into a single number that can be used to assess the state of the community
(Washington, 1984).
Different types of diversity indices have been developed to describe community structure (Pielou,
1975, Washington, 1984):
diversity indices that express the richness and variety of communities
evenness indices (similarity indices), that express the similarity (equitability) of communities
dominance indices, that emphasise the most important species in the community
biotic indices, that are used for estimating the degree of water pollution based on indicator
species.
Phytoplankton indices, to be useful in describing eutrophication pressure, must be sensitive to
changes in phytoplankton community structure, robust to the requirements of statistical analyses
and be effective in distinguishing different trophic conditions (Tsirtsis and Karydis, 1998). Various
indices have been tested in coastal areas, but many have not been proven to be consistent and
sufciently sensitive to be applicable for assessment of the impact of nutrient pressure on
phytoplankton.
A major problem in the use of phytoplankton diversity indices is that they are extremely dependent
on taxonomic resolution and consistency of microscopical analysis, as well as the level of
taxonomical knowledge. When using indices in which the number of species plays the central role,
exclusion of rare species, either by insufcient taxonomical expertise or by small sample size, may
seriously violate the reliability and sensitivity of an index (Cao et al., 1998).
1
See Annex 1 for a list of common diversity indices and their formulas.
44 |
Characterization of the Baltic Sea Ecosystem: Dynamics and Function of Coastal Types (EVK3-CT-2001-00065, 2001-2004).
45
In temperate and high latitudes, the annually occurring spring bloom, consisting usually of
diatoms, is a normal phenomenon and part of seasonal plankton succession (Smayda, 1997). The
spring bloom is essential in the seasonal succession, as it serves as a signicant source of food for
zooplankton and bottom fauna. However, with eutrophication, the intensity of the spring bloom
is augmented, and the increasing biomass leads to increased amounts of organic matter settling
to the bottom. Decomposition of organic matter by bacteria consumes oxygen, leading in some
areas to deoxygenated sediments and bottom waters.
In contrast, episodic phytoplankton summer blooms occur as a response to pulses of new
nutrients or a reduction in grazing pressure and can be classied as exceptional (Smayda, 1997).
Some of these blooms are harmful, i.e. they either produce high biomass leading to detrimental
ecosystem effects per se, or by being toxic, causing mortality of sh and other organisms. Moreover,
toxic bloom events pose a serious health risk for humans when algal toxins are concentrated in
shellsh cultivated for human consumption (Cloern, 2001; Granli, 2004). Toxic blooms cause
considerable economic harm on a global scale as well as in European coastal zones (Cloern,
2001). Most harmful algal blooms (HABs) in coastal areas are caused by microalgae (20-200 m
in size; Moestrup, 2004). HABs can be composed of different taxonomic groups, of which
dinoagellates are the most numerous (Dinophyta: 69 species). Other groups represented are
diatoms (Bacillariophyta: 12 species), haptophytes (Haptophyceae: 9 species) and rapidophyceans
(Rapidophyceae: 7 species; Moestrup, 2004). Although a direct causal connection between
eutrophication and increased frequency of harmful algal blooms has not been proven, it is
generally believed that their frequencies have increased worldwide due to increased nutrient
input (Hallegraeff, 1993; Anderson et al., 2002; Granli, 2004).
Bloom denition. When discussing episodic phytoplankton blooms, the term phytoplankton
bloom needs to be dened before it can be used in an operational, or even in a conceptual way.
Blooms can be considered to be exceptional, unusual and nuisance and can be dened in
many ways (Smayda, 1997). For example, a bloom is a deviation from the normal cycle of
phytoplankton biomass (Parker, 1987), or a period when chlorophyll-a concentration exceeds
100 mg m-3 (Tett, 1987).
Carstensen et al. (2004) have developed an operational denition that is useful for assessing the
frequency of phytoplankton summer blooms, i.e. other than the spring bloom. Their numerical
denition is based on monitoring data of chlorophyll-a, accompanied with information on
phytoplankton composition. They dene a bloom statistically as percentage of observations
where a station-specic chlorophyll-a concentration is outside the Gaussian distribution of
observations. This approach is potentially useful in assessing the status of coastal waters based
on anomalies in bloom frequencies as required by the WFD.
However, in many harmful algal blooms, the abundance or biomass of the causative organism (often
dinoagellates or diatoms) is relatively low, but are considered harmful because of toxin accumulation
in sh or shellsh that lter the toxic cells for food (Smayda, 1997). On the other hand, extensive kills
of sh and bottom fauna are often connected to high biomasses of toxic haptophytes (Dahl et al.,
1989). But even so, harmful blooms are often temporally and spatially restricted, and their detection
using conventional monitoring methods is difcult as well as stochastic.
46 |
47
Table 2.1 Examples of empirical models on phytoplankton and nutrients, developed for European
coastal areas.
Brief model characteristics
Area applied to
Reference
Danish estuaries
(< 8.5 m depth)
48 |
Table 2.2 Examples of deterministic models on phytoplankton and nutrients, developed for
European coastal areas.
Brief model characteristics
Area applied to
Reference
NW Black Sea
Szczecin lagoon,
Poland
(Dippner, 1998)
North Sea
Continued
49
Area applied to
Reference
Generic
North Sea
Mediterranean Arabian
Sea
Generic
Estuaries
Oceans
English Channel
Bay of Biscay
Generic,
Dutch coastal waters
Continued
50 |
The NORWegian ECOlogical Model system is a coupled 3D physical-chemicalbiological model system applied to study primary production, dispersion of
particles (sh larvae, pollution) and eutrophication. The biological-chemical
module simulates subsurface light, two groups of phytoplankton (diatoms and
agellates), and their growth as affected by nutrient concentrations, light
intensity and temperature. The model does not include zooplankton as a state
variable but instead a constant death rate of phytoplankton (which is also
assumed to include grazing) is included.
The MIKE EU/MIKE EcoLab Eutrophication Template describes nutrient cycling,
phytoplankton and zooplankton growth, growth and distribution of rooted
vegetation and macroalgae in addition to simulating oxygen conditions. The
eutrophication module is seamlessly integrated with the (1-, 2-, 3D) advectiondispersion modules, which describes the physical transport process at each gridpoint covering the area of interest. The EcoLab allows the user to add new state
variables and modify process descriptions.
Review of deterministic models covering the North Sea.
North Sea
Skagerrak and
Kattegat.
Generic
DHI:
download description in
http://www.dhisoftware.
com/ecolab/
(Moll and Radach, 2003)
Classication schemes
OECD classication. The OECD has recommended a classication system for trophic conditions
in lakes, rivers and reservoirs (Vollenweider and Kerekes, 1982). The classication is based on
probability distributions of easily analysable variables describing pressures (concentrations of
total N and total P) and phytoplankton biomass (chlorophyll-a concentration, peaks in chl-a, and
transparency i.e. Secchi depth), and it sets boundaries to ve trophic categories from ultraoligotrophic to hypertrophic. Weaknesses in this classication scheme are: 1) There is considerable
overlap in the probability distributions, which makes the boundary setting difcult. On the other
hand, the probabilities illustrate the uncertainty of the classication; 2) The probabilities are set
by each variable individually, and these criteria may be controversial; 3) The scheme presumes
that the environment is homogenous and in a stable state.
The OECD classication scheme was further developed by Zurlini (1996) and applied to the
coastal waters of the Adriatic Sea, Mediterranean. The approach was based on combining the
distinct probabilities introduced in the OECD scheme (TN, TP, Chl-a, transparency). The work
showed that classication uncertainties, caused by the uncoupling of trophic variables are related
to environmental disturbances by discharges, inows and turbulence.
Trophic status index. A trophic status index (TSI), developed by Carlson (1977) for lakes, denes
each trophic state by a doubling of phytoplankton biomass, measured with Secchi disk transparency,
and relating that to total phosphorus concentration (Carlson, 1977).
The Carlson index was the basis for the TRIX index, developed for the coastal marine environment
by Vollenweider et al. (1998). The TRIX index includes chlorophyll-a and oxygen saturation (in
percentage; expressing phytoplankton productivity), concentrations of total N and total P,
available DIN and DIP (expressing nutritional factors), and transparency (as a supplementary
water quality factor). The latter gives the possibility to include turbidity caused by factors (minerals,
dissolved substances) other than phytoplankton in the calculation of the TRIX index. The TRIX
51
index can be useful in classication, especially when complemented with the N:P ratio, or other
additional information (Vollenweider et al., 1998). The TRIX index has been tested by Moncheva
et al. (2002) for a coastal region of the Black Sea with promising results.
Vollenweider et al. (1998) note that when trying to transfer limnological models to marine
conditions, it is necessary to take into account some basic characteristics that differ between lake
and marine ecosystems. First of all, whereas limnological criteria characterise lakes as an entity
(i.e. the trophic status is assigned on a whole lake basis), this concept is not applicable in marine
environments (except possibly in enclosed bays and lagoons), where prevailing currents, inshoreoffshore exchange, tidal forcing, and upwellings continuously modify the physico-chemical and
biological patterns in time and space.
OSPAR classication. The OSPAR commission has agreed upon classication of NW Atlantic seas,
including the North Sea and the Celtic Sea, into three classes with respect to eutrophication:
1) problem areas, 2) potential problem areas and 3) non-problem areas (OSPAR, 2003).
For phytoplankton, the classication criteria set to reect direct effects of nutrient enrichment
include maximum and mean chlorophyll-a concentration (elevated level of chl-a concentration is
dened as >50% above offshore or historical concentrations), and region/area -specic
phytoplankton indicator species (elevated nuisance bloom or toxic assessment levels). The indicator
species are categorized as 1) nuisance species, which cause nuisance, foam or oxygen deciency
(e.g. Noctiluca scintillans and Phaeocystis spp. in colony form), and 2) toxin producing species,
which cause sh and benthos kills or PSP and DSP3 contamination in mussels (e.g. Chrysochromulina
polylepis, Gymnodinum mikimotoi, Alexandrium spp., Dinophysis spp. and Prorocentrum spp.;
OSPAR, 2003). Indirect and other possible effects of nutrient enrichment include oxygen deciency
(<2 mg l-1 acute toxicity, 2-6 mg l-1 deciency), and algal toxins (DSP/PSP mussel infection events).
Other classication schemes. All estuaries draining from the UK mainland have been classied
according to their annual nutrient loads, water ow and tidal action by Nedwell et al. (2002).
They concluded that chlorophyll level does not directly indicate nutrient loading to the estuaries,
because it is also inuenced by physical constraints and turbidity caused by suspended solids.
A WFD-based classication of the ecological status of coastal waters has been done in Basque country
(Borja et al., 2004a,b) which proposes EQR thresholds to be used for each ecological status level.
In the Netherlands three classication methods have been developed. The schemes have been
developed for all aspects of coastal ecosystems. The classication systems for the phytoplankton
element are:
1) AMOEBE. The AMOEBE indicator system uses the percent abundance of indicator species
as a percentage of the abundance under reference conditions (1930) as an indicator for the
health of the North Sea ecosystem (Baptist and Jagtman, 1997). For phytoplankton two
indicators are used: averaged total phytoplankton biomass and Phaeocystis.
2) GONZ. In the GONZ system (Kabuta and Duijts, 2000) there are 3 phytoplankton-related
indicators: 1) phytoplankton species diversity (indicated by Shannon Wiener index:
monospecic bloom = 0, even distribution over many species = 1); 2) phytoplankton structure
3
52 |
(indicated by N:P ratio: (DIN:DIP winter average and summer average); and 3) primary
production (calculated with GEM model, corrected for natural variability in meteorological
conditions and river discharges).
3) Ecosystem targets North Sea. As part of the Ecosystem targets North Sea (Boon and
Wiersinga, 2002) 11 indicators related to phytoplankton are used to evaluate if target
values are met: DIN and DIP concentrations, N:P ratio, chlorophyll-a, oxygen concentration,
selected species as indicators: Karenia mikimotoi, Dinophysis spp., Alexandrium spp.,
Pseudo-nitzschia spp., Phaeocystis globosa, and state of ship ballast water.
2.3 Macrophytes
Introduction
Benthic macrophytes in coastal and transitional waters include macroalgae and seagrasses and,
in brackish areas a few genera of salinity-tolerant angiosperms other than seagrasses
(e.g. Potamogeton, Zannichellia, Ruppia). Benthic macrophytes have a lifetime of months to years
and most species grow at the same spot attached to the bottom substratum. Their growth pattern
therefore reects a time-integrated response to physical and chemical characteristics of the
habitat. Seagrasses and different algal species or functional algal groups have different nutrient
demands and changes in nutrient concentration therefore affect dominance patterns of the
benthic vegetation as well as dominance patterns between planktonic algae and benthic
vegetation (Sand-Jensen and Borum, 1991; Duarte, 1995; Pedersen, 1995).
Planktonic algae and opportunistic macroalgae are generally favoured by high nutrient
concentration. When phytoplankton biomass increases the depth distribution of seagrasses and
perennial macroalgae decreases due to shading and ultimately benthic plants may disappear
(Duarte, 1995). Nutrient and transparency conditions thereby often exert combined pressures on
the benthic vegetation. Other physico-chemical factors such as salinity, physical exposure and
substrate composition as well as biological factors like grazing or contagious diseases may also
affect growth- and loss processes and may complicate the interpretation of causes of changes in
benthic vegetation (Schramm, 1999). The analysis of cause- and effect relationships is rendered
even more complex because of possible negative feed-back effects of eutrophication which may
accelerate the loss of benthic macrophytes and delay restoration (Duarte, 1995; Figure 2.6).
Seagrass meadows and benthic algal communities such as perennial kelp forests are appreciated
mainly because of the services they provide to overall functioning of coastal ecosystems (see
details regarding seagrasses in Hemminga and Duarte (2000): 1) they enhance biodiversity and
habitat diversity by providing possibility for attachment, refuge and food resources; 2) they
improve water quality by reducing particle loads in the water and absorbing dissolved nutrients,
and by promoting sedimentation of suspended particles; 3) they stabilise sediments due to
underground networks of seagrass rhizomes and roots and due to a reduced ow regime inside
the canopies which diminishes sediment resuspension; 4) they play a signicant role in global
carbon and nutrient cycling. Benthic plants constitute an important sink for carbon in the oceans
(Smith, 1981) because of their high levels of biomass and production and because most of the
biomass of seagrasses ends up as refractory detritus. In an assessment of the economic value of
Nutrient
load
53
Grazing
Plankton &
opportunistic
algae
Turbidity
Benthic resp.
Oxygen
Seagrasses &
perennial
macroalgae
Erosion &
resuspension
Figure 2.6 A cartoon depicting a conceptual model of the effect of increased nutrient loading on
submerged vegetation, stressing the self-accelerating nature of the process and the buffer mechanisms
operating. Redrawn and modied after Duarte (1995).
the worlds ecosystems, the value of the nutrient cycling function of seagrass beds and beds of
macroalgae ranked second among the listed ecosystem values (Costanza et al., 1997).
Changed dominance patterns of the coastal primary producers from benthic macrophytes to
planktonic algae or from long-lived seagrasses and macroalgae towards opportunistic algae as a
consequence of increased nutrient concentrations and reduced water transparency may affect the
above-mentioned functional attributes. Moreover, opportunistic algae grow and decompose faster
than perennial species and may thereby generate a temporal imbalance between oxygen
production and consumption increasing the likelihood of anoxia (Sand-Jensen and Borum, 1991).
Blooms of lamentous algae also reduce the recreational value of coastal waters as they
accumulate in the water column and on the beach and anoxic events associated with macroalgal
blooms have negative effects on the ecosystem (Valiela et al., 1997).
54 |
Although highly signicant, the relationships typically show a wide scatter. The models are
therefore best suited for describing mean expected depth limits at given levels of nutrient
concentration/transparency rather than providing precise estimates for specic areas (Nielsen
et al., 2002a; Sagert et al., 2005; Greve and Krause-Jensen, 2005). The wide scatter in the
relationships indicates that factors other than light and nutrients contribute to regulating depth
limits. Sediment characteristics are, for example, likely to play a role in this regulation.
Recent scientic results suggest that oxygen deciency may harm seagrasses (Terrados et al.,
1999; Holmer and Bondgaard, 2001; Koch, 2001; Greve et al., 2003) and reduced, organic rich
sediments prone to oxygen deciency might therefore hinder seagrass growth. Sediment
characteristics can also affect algal depth limits since lack of hard substratum may limit depth
penetration in some areas.
Table 2.3 Relationships between depth limits of coastal macrophytes and water quality.
Indicator
Area applied to
Independent variables
Woods Hole, MA
World wide
Danish coastal waters
Danish coastal waters
Danish coastal waters (1994)
World wide
General
General
55
Regarding macroalgae, the best relations between depth limits and water quality have been
developed for the algal community as a whole and for larger algal groups (e.g. brown algae).
Models have also been attempted for depth limits of key algal species like Fucus vesiculosus in the
Baltic Sea (Table 2.3). The best correlation between F. vesiculosus depth limit and transparency
was found for a restricted area of low salinity (Kautsky, 1999), while only very weak relationships
were found for high salinity regions at the entrance of the Baltic Sea (Torn et al., 2006). These
divergences are partly explained by large salinity-related changes in algal depth limits (Pedersen
and Snoeijs, 2001): At high salinity, species diversity is high and inter-specic competition forces
F. vesiculosus to colonize shallow water where light is not a limiting factor. As salinity declines,
species diversity is reduced and F. vesiculosus can penetrate to deeper, more light limited waters.
The marked inuence of salinity implies that depth limits of individual algal species are highly
area specic indicators and indicator levels should accordingly be dened for specic areas.
Empirical relation
Zc = 1.62/K
log Zc = 0.27-0.84log K
ln Zc = 6.039 0.755ln(TN)
Zc = 0.339 + 0.786Zs
Zc = 2.44 + 0.11Zmax 0.87NH4+ + 0.26Zs-winter
Zc = 1.27 + 0.06Zmax 0.15NH4+ + 0.38Zs-summer
Zc = 0.97 + 1,06Zs
Zc = 5.361 * (TP)-1.86
Zc = 659.4 * (TP)-1.456
Not dened
Statistical data
R2 = 0.40, N = 29, p < 0.001
R2 = 0.55, N = 128, p < 0.0001
R2 = 0.61, N = 101, p < 0.0001
R2 = 0.71, N = 46, p < 0.001
(manual backward elimination)
R2 = 0.42, N = 390, p < 0.001
(manual backward elimination)
R2 = 0.668
R2 = 0.602
R2 = 0.632
R2 = 0.78, N = 8
R2 = 0.87, N = 8
R2 = 0.91, N = 8
R2 = 0.93, N = 8
R2 = 0.88, N = 8
R2 = 0.77, N = 72, p < 0.001, SEslope = 0.07
Reference
(Dennison, 1987)
(Duarte, 1991)
(Nielsen et al., 2002b)
(Nielsen et al., 2002b)
(Greve and Krause-Jensen, 2005)
(Greve and Krause-Jensen, 2005)
(Sagert et al., 2005)
(Abal and Dennison, 1996)
(Duarte, 1991)
(Koch, 2001)
(Koch, 2001)
56 |
Abundance at specic depths. The abundance of seagrasses and macroalgae can be measured
in terms of cover, biomass and (for seagrasses also) shoot density at specic water depths.
Abundance is typically quite variable in shallow areas where exposure to wind and waves plays a
major regulating role, but from intermediate water depths towards deeper water abundance tends
to decline in parallel to reductions in light availability with depth (Duarte, 1991; Krause-Jensen
et al., 2000; Dahl et al., 2001; Krause-Jensen et al., 2003). Vegetation abundance at specic
depths therefore responds to changes in nutrient levels and transparency and this relationship has
been described in several models (Table 2.4).
Total cover of macroalgal communities on Danish stone reefs declines with depth and this decline
has been shown to be most marked in years with high nutrient load (Dahl et al., 2001). Cover of
macroalgal communities along the Danish coasts is also highest in the clearest waters with lowest
nutrient concentration and declines towards more nutrient rich areas. However, while coastal
macroalgal cover responds to large-scale differences in water quality between areas, the indicator
is not sufciently sensitive to reect smaller year-to-year changes in water quality (Krause-Jensen
et al., in press). More studies of factors regulating algal cover are needed to make dose-response
relationships generally applicable.
Table 2.4 Relations between abundance of coastal macrophytes at specic depths and water quality.
Indicator
Area
applied to
Independent variables
Empirical relation
Seagrass abundance:
downward slope/
attenuation of
seagrass biomass
(Kbio, m-1)
Eelgrass abundance:
probability of eelgrass
cover
Worldwide
light attenuation
(K, m-1)
Macroalgal
abundance: total
algal cover (modelled
average) (TC, %)
Danish coastal
waters: 0-1m,
1-2m, 2-4m,
4-8m
Danish stone
reefs
TC=3.6898-0.5973ZmaxXxTNxlocality, where X
depends on locality
(see paper)
TC=-0.386+0.0407Zs+
0.0205S-0.419L
Statistical
data
Reference
See paper
(Krause-Jensen et
al., 2003)
See paper
R2=0.79,
N=28,
p<0.05
(Krause-Jensen et
al., in press)
57
In Greek coastal waters, cover of opportunistic algae relative to cover of late successional species
including seagrasses and perennial macroalgae has been suggested as an indicator of water
quality (Orfanidis et al., 2001; 2003). This indicator was tested in Danish coastal waters, but here
the relative abundance of opportunistic algae was more closely related to differences in salinity
than to differences in water quality between areas (Table 2.5).
There are indications that the relative abundance of green opportunists alone may be a more
sensitive indicator than the entire group of opportunists. A recent mesocosm experiment showed
no overall increase in the abundance of opportunistic algae along an articial eutrophication
gradient, but instead demonstrated a change in the composition of opportunistic algae from
dominance of corticated lamentous red algae to dominance of thin foliose green algae (Karez
et al., 2004). Middelboe and Sand-Jensen (2000) also found an increase in the relative abundance
of opportunistic green algae and a decline in large perennial brown algae following increases in
nutrient concentrations in a Danish estuary over a 50-year period.
The abundance of opportunistic macroalgae is extremely dynamic. The algae have fast growth
and decay rates and as they often occur free-oating, their distribution and abundance vary
depending on wind events. Moreover, differences in grazing pressure may markedly affect their
abundance (Geertz-Hansen et al., 1993). Such a dynamic nature is a hindrance for precise
prediction of abundance levels and suggests that a dense net of sampling stations with frequent
sampling is necessary in order to assess abundance.
Changes in the composition and dominance patterns of benthic vegetation in response to changes
in nutrient/transparency levels have also been described at the species level. One example is from
brackish German boddens where the composition of macrophyte communities has been described
for different water quality regimes (Blmel et al., 2002; Blmel et al., 2004). Differences in species
composition of macrophytes as a function of nutrient level has also been used in a saprobia
classication of Finnish coastal waters (Blomster, 1996; Viitasalo et al., 2002; Hllfors et al.,
1987). In the UK, species composition of macroalgal communities is also used in the classication
of water quality (Wilkinson and Wood, 2003).
Table 2.5 Relations between relative abundance of opportunistic macroalgae (Op, in percentage) and
water quality. Indicator: relative abundance of opportunistic macroalgae (modelled average).
Area applied to
Waquoit Bay, MA
N-input (TN, ton year ) See paper
Danish coastal waters salinity (S)
Op=1.06+0.032S
No relation to water quality found
-1
Statistical data
Reference
R = 0.51, N = 5
R2 = 0.73, N = 28,
p < 0.0001
58 |
response to increased nutrient load because nutrient addition stimulates growth and standing
stock of algae which shade the seagrasses (Short and Burdick, 1996; Hauxwell et al., 2001;
Hauxwell et al., 2003). There is also substantial evidence that a serious decline in the depth and
area distribution of seagrasses in Dutch coastal waters is partly related to the increased nutrient
load and reduced transparency (Philippart, 1994). The best relations between water quality and
area distribution of seagrasses are likely to exist for relatively deeply located populations whereas
shallow populations which are not strongly light regulated may not be tightly related to changes
in nutrient load and water quality. Analyses of long-term changes in area cover of shallow Danish
eelgrass populations thus showed no relation to changes in nutrient load, probably because
stochastic events like storms and ice scour play a major role (Frederiksen et al., 2004a; 2004b).
In the Dutch Wadden Sea habitat characteristics like exposure levels, substrate characteristics and
salinity have been used to model the potential areal distribution of seagrasses (Philippart et al.,
1992; deJonge et al., 1997; deJonge and deJong, 1999; RIKZ, 2004).
Table 2.6 Relations between area distribution of eelgrass and water quality. Indicator: area distribution of
eelgrass (area, %).
Area applied to
Waquoit Bay, MA
Statistical data
Nitrogen load
Log area = 1.648 Nload
R = 0.88, p < 0.05
(Nload, kg km-2 y-1)
Waquoit Bay, MA
Nitrogen load
Area = 31(log Nload) + 54 R2 = 0.88, p < 0.05,
(Nload, kg ha-1 y-1)
n=7
Danish coastal waters Nload, insolation, wind No relation found
2
Reference
(Short and Burdick, 1996)
(Hauxwell et al., 2003)
(Frederiksen et al., 2004a)
59
results from particular characteristics of benthic fauna: 1) Animals are in contact with sediments
(which are recognised as a sink for many contaminants); 2) They play an important role in the
cycling of nutrients and certain contaminants; 3) Benthic animals are relatively sedentary and
long-lived and thus provide a measure of contaminant effects integrated over time; 4) They are
sensitive to anthropogenic activities and respond in a rather predictable way; 5) Benthic animals
are a commercially valuable resource or are relevant food sources for economically or recreationally
important species (Rees et al., 1990; Dauer, 1993). Therefore, especially concerning the latter
characteristic, the depletion of benthic communities following sediment contamination, dredging
or bottom trawling may represent an important socio-economic problem since they directly or
indirectly support several human activities (Rhoads et al., 1978; Chapman et al., 1987; Rees et al.,
1990; Kaiser et al., 2000).
Multivariate analysis
Multivariate methods are considered to be more sensitive than univariate measures for detecting
differences in community structure between samples, both in space and time (Clarke and Warwick,
1994). The most commonly used methods in macrobenthic community studies are hierarchical
clustering, non-metric multi-dimensional scaling (MDS), principal components analysis (PCA), and
60 |
correspondence analysis (CA). Nevertheless, these methods only assess differences between
communities and cannot be used as measures of community stress (Clarke and Warwick, 1994).
Benthic communities show great variability at regional scales resulting from natural environmental
conditions that, however, can be overcome by working at taxonomic levels higher than species
(Clarke and Warwick, 1994). The phylum meta-analysis approach uses an approximated value of
production provided by both abundance and biomass data. This approach was applied to NE
Atlantic fauna in disturbed and undisturbed areas. Although it may not be highly sensitive to
detect low-level or subtle perturbations, this technique seems to retain much of the sensitivity of
multivariate methods (Clarke and Warwick, 1994), and it can be useful, especially concerning the
study of wide-ranging areas. Savage et al. (2001) suggested that the phylum-level meta-analysis
appears to be better in assessing the impact of organic and chemical pollution on an ocean-basin
scale than physical disturbance due to offshore mining.
Classication schemes
Abundance/Biomass Comparison Curves ABC. ABC (Warwick, 1986) is a graphical method
that directly compares abundance and biomass K-dominance curves and has been applied
worldwide (Warwick et al., 1987; Weston, 1990; Simboura et al., 1995; Kaiser et al., 2000).
The method is based on the assumption that the distribution of numbers of individuals and
biomass among species within a community show a different response to disturbance (Warwick
et al., 1987). There are, however, some precautions to be followed when applying this method and
interpreting the results: 1) it should not be used in intertidal communities without reference to a
long-term and special series of control samples (Beukema, 1998); and 2) similar results may be
obtained for disturbed and undisturbed conditions e.g. after recruitment events (Warwick and
Ruswahyuni, 1987). With ABC Curves it is possible to recognise three different conditions
(undisturbed, moderately disturbed and grossly disturbed) in a community without reference to a
control area both in time and space. In undisturbed communities, the K-dominance curve for
biomass lies above the abundance curve for its entire length. Under moderate disturbance, both
curves are closely coincident and may cross each other one or more times. In grossly disturbed
communities the abundance curve lies above biomass throughout its length (Warwick, 1993).
Benthic Habitat Quality (BHQ) index. This index (Nilsson and Rosenberg, 1997) uses sediment
prole images to assign sediment quality and biogenic structures to 4 different successional
stages (SS 0 to SSIII). The method uses the redox potential discontinuity (RPD) layer and the
presence of burrows and animal tubes as an indicator of hypoxic conditions. Instead of the
separation into four successional stages, Rosenberg et al. (2004) suggested that this index should
be divided into 5 classes in order to be in agreement with the Water Framework Directive (WFD).
This index varies between 0 and 15 where high scores are assigned to mature successional stages
and low values with pioneering stages or azoic bottoms (Rosenberg et al., 2004).
Marine Biotic Index (BI). The marine biotic index (Borja et al., 2000) is derived from separating
the proportional abundance of individuals into ve ecological groups, which are related to the
degree of sensitivity/tolerance to an environmental stress gradient. In comparison to the biological
indices proposed previously (Hily et al., 1986; Grall and Glmarec, 1997), BI uses a mathematical
formula to obtain a continuous value the Biotic Coefcient (BC), which is more suitable for
61
statistical analysis. The BI value represents the quality of the bottom conditions in a discreet
range from 0 (unpolluted) to 7 (extremely polluted), according to the BC value.
BC = (( 0 %GI ) + (1. 5 %GII ) + ( 3 %GIII ) + ( 4. 5 %GIV ) + ( 6 %GV )) /100
where GI comprises very sensitive species; GII indifferent species; GIII tolerant species; GIV
second-order opportunistic species; GV rst-order opportunistic species, according to their
sensitivity to increasing pollution gradients. Information about the sensitivity of more than 2700
taxa from European and Mediterranean soft-bottom environments is available in AZTIs web page
(http://www.azti.es).
Borja et al. (2004a, b) presented some of the problems associated with the AMBI tool. The validation
of model development showed that different anthropogenic disturbances in the environment can
be detected through the use of the BI, such as dredging works, sewage loading or mud disposal.
According to Borja et al. (2000), the BI can be applied when attempting to determine the ecological
status of European coastlines. Nevertheless Simbura and Zenetos (2002) have identied some
discrepancies when using this index on Mediterranean samples, and they suggest that the BI is
more appropriate for Atlantic ecosystems and estuarine areas (Simboura, 2004).
Benthic Index of Biotic Integrity (B-IBI). This index (Weisberg et al., 1997) compiles a number of
measures into a single score of benthic community health. Included in calculating the B-IBI are
measures of species diversity, species composition (e.g. % abundance and biomass, pollution
sensitive taxa), productivity, trophic composition (e.g. % deep deposit-feeders) and the depth
distribution of taxa and biomass in the sediment. The index was developed for the Chesapeake
Bay, USA using reference sites and ranges from 1 to 5 (in later versions the scale is extended to
between 1 (poor) and 10 (high quality), and has been used routinely in Chesapeake Bay monitoring
since 1999.
BQI = ( (
i =1
Ai
ES500. 05i )) 10 log( S + 1) ,
totA
where A is the mean relative abundance of a species i; S is the mean number of species at a
station.
Exergy index. The exergy index has been used in several studies as an ecological organizing
principle (Xu et al., 1999; Jrgensen and Marques, 2001; Marques and Jrgensen, 2002). Exergy
can be dened as the amount of work that can be extracted from a system when brought into
thermodynamic equilibrium with its environment. This includes both an energetic and information
content embedded in the biomass, which has been estimated by the complexity of the organisms
DNA. The total exergy is the sum of the compartmental biomasses multiplied by an organism
specic weighting factor. Standard values for these weighting factors are available in the literature
62 |
for a variety of organisms (Jrgensen and Marques, 2001; Marques and Jrgensen, 2002). Fabiano
et al. (2004) concluded that exergy appeared to be sensitive to changes in environmental
conditions and trophic state and may therefore be proposed as a useful tool for the health
assessment of marine benthic ecosystems.
The WFD requires that the environmental quality assessment of coastal ecosystems comprises 5
classes of quality status: Bad, Poor, Moderate, Good, and High. Three of the indices
discussed above (BQI, BHQ and BI) were adapted in order to be in agreement with this classication
and are summarised in Table 2.7.
Table 2.7 Correspondence between Environmental quality status as described in WFD and three benthic
indices BQI, BHQ and BI values (see text).
HIGH
All the
disturbancesensitive taxa
WFD
associated with
undisturbed
conditions are
present
BQI 20 m 14.4
BQI > 20 m 16.0
BHQ 20 m 15.0 - > 8.0
BHQ > 20 m 15.0 - > 11.0
BI
0 - 1.2
Dominant
EGI
Ecological
Species very
Groups (Borja sensitive to
et al., 2004) pollution
GOOD
MODERATE
POOR
BAD
Most of the
sensitive taxa of
the type-specic
communities are
present
Taxa indicative of
pollution are present.
Many of the sensitive
taxa of the type-specic
communities are present
biological communities
deviate substantially
from those normally
associated with the
surface water body type
under undisturbed
conditions
< 7.2 - 3.6
< 8.0 - 4.0
4.0 - > 2.0
4.0 - > 2.0
> 4.3 - 5.5
Models
Models simulating the impact of different disturbance types on the macrofaunal community can
be divided into three main categories: 1) screening models, 2) empirical models (PearsonRosenberg and bethic-TOC; see below), 3) ecological or food-web models.
Screening models. A Geographic Information System (GIS) is a powerful management tool that
allows the integration of all information for a given area. Due to the high complexity of marine
and estuarine areas, GIS offers a good way to visualise, organise, combine and analyse data.
Pearson-Rosenberg model. This model (Pearson and Rosenberg, 1978) is based on species
richness, abundance, and biomass (SAB). This is probably the most commonly cited model and
predicts a specic sequence of successional stages after disturbance. It predicts that an increase
in disturbance results in an increase in the number of species and biomass. After an initial increase,
63
both variables decrease to the ecotone point, followed by a secondary maximum of biomass and
abundance associated with a few opportunistic species. Under extreme conditions the community
may attain an azoic state. Although it is applied worldwide, results from other studies indicate
that predictions from this model can be quite variable; therefore it must be applied with caution
(Smith and Brumsickle, 1989; Thrush et al., 1996).
Benthic-TOC relationships. A model for the macrobenthic fauna and total organic carbon (TOC)
relationships (Hyland et al., 2000) has been produced based on the Pearson and Rosenberg
model (Pearson and Rosenberg, 1978). According to the benthic-TOC model, benthic variables
(number of species, abundance, and biomass) would increase up to a certain critical level in
relation to a sediments increasing organic carbon content (TOC) declining afterwards. Population
increases below this TOC critical level reect a combination of the nutritional value of moderate
levels of organic matter present in the sediment and other favourable environmental conditions,
such as sufciently high levels of dissolved oxygen and low sediment-associated stressors
(contaminants, ammonia, sulphide). As TOC exceeds a certain critical level, the benthos is exposed
to increasing amounts of physiological stress resulting from oxygen depletion and increasing
concentrations of contaminants or other sediment-associated stressors.
Ecological models. Several ecological models have been used to evaluate the impact of
anthropogenic activities in marine ecosystems, mainly sheries. Basically, the models can be split
into seven categories, depending both on the required input variable data and produced output
predictions (ICES, 2000). According to Robinson and Frid (2003), the categories are:
Habitat-based models including those that give an insight into how a population range will
t to the most suitable habitat as shing changes the total habitat size.
Models based on community metrics; these are models that reect how community-level
metrics change in response to shing disturbance.
Single-species models with variable prey or predators incorporating one-way trophic feedback
reactions on dynamic single-species models following a shery disturbance.
Multispecies production models are those that show how shery harvest of predator or prey
will affect the abundance of the other.
Dynamic multispecies models can incorporate spatially dynamic or age/size-structured
populations into changes in predatorprey interactions brought about by shing disturbance.
Aggregate ecosystem models derive from food webs and energy budgets, illustrating changes
in energy, carbon or biomass of aggregated functional species groups.
Ecosystem models with age/size structure, distinguishable from aggregate ecosystem models
in that the individual functional groups are generally less aggregated and there is greater
temporal resolution in their dynamics.
Among these categories, the ecological models that proved to yield good insights were those
categorised as aggregate ecosystem models and ecosystem age/size structures. Usually, these
kinds of models are derivates of the ECOPATH with Ecosim modelling approach.
The Ecopath with Ecosim (EwE). This modelling approach combines software for ecosystem
trophic mass balance analysis (Ecopath), with a dynamic modelling capability (Ecosim) for
64 |
exploring past and future impacts of shing and environmental disturbances as well as for
exploring optimal shing policies. Ecopath with Ecosim(EwE) is being widely used as a tool for
analysis of exploited aquatic ecosystems, but EwE can produce misleading predictions about the
direction of impacts of policy proposals. Erroneous predictions usually result from bad estimates
or errors of omission for a few key parameters, rather than diffuse effects of uncertainties in all
the input information (Christensen and Walters, 2004).
2.5 Summary
Phytoplankton. Coastal and transitional waters are the recipients of land-based nutrients, and
thus integrate nutrient loads from various sources. As the phytoplankton blooms have been
intensifying in many coastal areas, so too has the research effort to understand the factors
governing the initiation and fate of blooms during the last few decades. Despite the large amount
of results and literature available on phytoplankton and nutrients, region or coastal type-specic
dose-response relationships between nutrient concentrations and phytoplankton production have
only been described for some coastal areas. Such relationships, coupled with nutrient loading
models and appropriate phytoplankton status indicators are needed to allow WFD compliant
classication, and the setting of environmental objectives for different coastal areas, as a part of
river basin management programs and a program of measures.
WFD compliant classication systems are currently under development in many countries.
Currently, classication systems based on phytoplankton biomass and composition are only
developed for some parts of the NE Atlantic ecoregion. For most of the Baltic Sea and Mediterranean,
WFD compliant classication systems are not yet established.
Despite the increasing frequency, duration and coverage of algal blooms, little is known about the
factors that govern the initiation and taxonomic composition of blooms. It is not known what is
actually the role of nutrients in the blooms compared to other factors such as light, mixing,
nutrient composition, life cycles, etc. In addition, other agents such as dissolved organic matter
(e.g. humic substances) may be important for bloom initiation and success of toxic dinoagellates
(Doblin et al., 1999; Granli et al., 1999; Stolte et al., 2002).
Empirical, Vollenweider type models have not been developed for many coastal areas. Whereas in
lake ecosystems the Vollenweider model on the relationship between phosphorus loading and
phytoplankton biomass (chlorophyll-a) is applicable for 75% of lakes, it is not possible to develop
a common data-driven model for the interaction between one nutrient and phytoplankton
dynamics in coastal/estuarine ecosystems. This is mainly because nutrient limitation patterns are
variable across European coastal zones, as well as seasonally within a coastal area. Coastal areas
and estuaries respond to increased nutrient loading in different ways, depending on their
characteristic features that inuence their ability to buffer nutrient enrichments on the ecosystem
including different limitation patterns (N, P, Si, light, etc.). More information on the regional/
local nutrient limitation patterns and applicability of indicative nutrient ratios to predict the
changes in phytoplankton biomass and composition will be needed for development and
application of empirical dose-response models for European coastal areas.
65
There are a relatively large number of deterministic ecosystem models developed for European
coastal seas. Many of those simulate the development of phytoplankton biomass, and some are
also able to simulate changes in phytoplankton composition. Models that simulate both
parameters would be a helpful tool to develop WFD compliant classication systems, including
hind-casting or simulating reference conditions as well as setting the class boundaries with respect
to ecological discontinuities in the phytoplankton response curves. Such nonlinear points in doseresponse relationships that may lead to shifts between alternative stable states of an ecosystem
would be needed to set ecologically relevant class boundaries for WFD classication systems,
allowing scientic setting of the environmental objectives for good ecological quality. Identication
of such thresholds or point-of-no-return requires thorough understanding of the ecosystems
processes, bottlenecks in the resilience of the ecosystems and careful model formulation (Duarte,
2004). Furthermore, model testing and validation, with respect to monitoring alternative stages
in eutrophication in Europe, are restricted to the Baltic Sea area (Elmgren and Larsson, 1997; Rask
et al., 1999).
Macrophytes. This chapter demonstrates that coastal macrophytes do indeed respond to changes
in nutrient/transparency levels and therefore can be used as indicators of water quality. The best
empirical relations to water quality exist for deep communities because they are typically strongly
regulated by water transparency and only moderately by wave exposure. Existing relations do,
however, show considerable unexplained variation, which limit the predictive capacity of empirical
models. The variation can only be reduced by identifying its causes and including supplementary
regulating factors in future models. Several studies indicate that e.g. physical exposure, sediment
characteristics and occurrence of anoxic events may play signicant regulating roles. We encourage
further studies of such effects as well as analyses of possible negative feed-back effects of
eutrophication and identication of possible nutrient generated regime shifts in benthic
macrophyte communities.
Benthic invertebrates. Many of the techniques used in benthic ecology should be complementary,
as each only provides part of the complete information (Elliott, 1994). Macrofauna is recognised
as a proper tool for monitoring the environmental health of marine ecosystems, but studies on
this biotic component are highly labour intensive, both in terms of sampling effort and sample
processing (sorting and identication to species level). Therefore, several studies have focused on
the taxonomic resolution needed to assess environmental disturbances (Warwick, 1988; Somereld
and Clarke, 1995; Olsgard et al., 1997). According to these authors, for soft bottom macrobenthos
when using multivariate methods, disturbance effects are often detectable at high taxonomic
levels, such as the family level. Warwick (1993) also suggested that in environmental impact
studies, it would be more important to analyse a large number of stations/replicates at a higher
taxonomic level than a small number of stations at the species level.
Normally, for macrobenthos, there is a positive correlation between taxonomic groupings and
ecological functionality (Warwick, 1993). Several works have assessed macrobenthic impacts from
different sources of disturbance at high taxonomic levels (Bascom, 1982; Berge, 1990; Savage
et al., 2001). Nevertheless, Rosenberg et al. (2004) recommend the use of the highest possible
taxonomic level, as different species within the same genera may have different levels of tolerance
to disturbance. Independent of the taxonomic resolution applied, more information is needed
regarding the behaviour of benthic taxa, and not just whether they are sensitive or opportunistic.
66 |
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78 |
Annex to chapter2
Diversity indices used for phytoplankton community assessment
with respect to coastal eutrophication
( )
( )
(Karydis and Tsirtsis, 1996; Tsirtsis and Karydis,
1998;
= (Danilov
)
( )
1) Diversity indices
Simpsons D
Kothes species decit
Odums species per 1000 individuals
Gleasons D
Margalefs D
Menhinicks D
Shannons H
Brillouins H
Hills N 0
Hills N 1
Hills N 2
Hurlberts PIE
McIntoshs M
Keefes TU
(( ))
( )
(((())))
)
(((())
(
)) () )
(
=
=
(
)
( )
= =
=
==
=
=
=
=
=
=
=
S
=
(
)
(()==)
=
( )
( )
( )
( )
( )
) =
(
)(
(
= =
=
=
(
((
)
(
(( ( ))
((
)
( ( ))
) )
))
2) Evenness indices
Evenness E1
Evenness E2
COASTAL
Evenness E3
Evenness E4
Evenness E5
Redundancy R
Jaccards J
3) Dominance indices
Berger-Parker
McNaughtons
4) Saprobic indices
Saprobic index
5) Similarity indices
Gleasons SIGL
Kulczynskis SIKU
Ruzickas SIRU
Pandeyas SIPA
Ellenbergs SIEL
80 |
WITH
S
= the number of species in a sample or a population
N
= the number of individuals in a population or a community
Ni
= the number of individuals in a species i of a population or community
n
= the number of individuals in a sample from a population
ni
= the number of individuals in a species i of a sample from a population
pi
= ni /n = the fraction of a sample of individuals belonging to species I
Smax = the maximum number of species in a sample
n1, n2 = the number of individuals in the two most abundant species
Hmax = ln S (Pielou 1975)
Hmin = (1/N) * ln[N!/(N S + 1)] (Pielou 1975)
ti
= the number of species in the population i
tj
= the number of species in the population j
tc
= the number of species common in the populations I and j
K
= saprobic index
ki
= saprobic value of indicator species i
xi
= abundance of the ith phytoplankton species at site x
yi
= abundance of the ith phytoplankton species at site y
T
= subset of species occurring in both samples
U, V = subsets of species occurring only in one sample or the other
D1, D2 = Simpsons indices of the two samples
81
3.1 Introduction
The impacts of inorganic nutrient enrichment on river ecosystems are seen in many rivers and
have been intensively studied. For the implementation of the WFD it is equally important to be
able to also describe quantitatively the ecological consequences of reduced nutrient concentrations
in the different types of rivers to be able to decide on nutrient reductions necessary to meet WFD
quality objectives. Enrichment in inorganic phosphorus and nitrogen concentrations in rivers can
cause the following impacts, as summarised in Nijboer and Verdonschot (2004):
Increase in primary production rate and mass growth of algae and plants. Increase in
nutrients can potentially increase the growth of algae and macrophytes if these nutrients
were initially limiting and if the other in-stream conditions allow more growth (e.g. light).
Change in communities. A change in nutrients can lead to a shift from nutrient-sensitive
slow-growing species to nutrient-tolerant fast-growing species. This may result in competition
for light between epiphytes, macrophytes and phytoplankton, modifying the balance of these
algae and plants. This may have impacts on macroinvertebrates and sh through changes
to habitats and the food web.
Reduction in oxygen. High nutrient levels favour a high biomass of algae and plants.
Consequently, larger amounts of biomass are decomposed under oxygen consumption at a
later stage. A high autotrophic production of oxygen during the day is usually followed by a
high rate of respiration and often low oxygen concentration during the night. These processes
can lead to oxygen depletion in the water or in the sediment.
Nitrogen and phosphorus are naturally present in streams through transport of terrestrial organic
matter, leaching and runoff of terrestrial inorganic nutrients and deposition from the atmosphere.
Mainstone and Parr (2002) estimated that the background export rates of total phosphorus in
four UK rivers would be between 0.1 and 0.2 kg TP ha-1year-1, which means a total phosphorus
concentration level of 5-25 g l-1. All anthropogenic activities that release organic matter and
inorganic nutrients in the environment may cause in-stream enrichment in inorganic nutrients.
The predominant sources are population, industry, agriculture, transport and power plants.
In western countries the wastewater contribution from each person amounts to 1-1.5 kg P
capita-1.year-1 and 2.2 to 5.5 kg N capita-1.year-1. The main sources are excretion from the human
body and use of detergents (European Environment Agency, 1999). The wastewater nutrient
loadings to rivers depend mainly on the population density in the river catchment and the level
of nutrient removal at wastewater treatment plants. Depending on the treatment level, up to 95%
of the phosphorus can be removed from wastewaters (Brett et al., 1997).
Industries, primarily the food and drink industry, the industries producing phosphorus-based
fertilisers, cleaning materials, pesticides and/or metal nishing (Morse et al., 1993), can discharge
signicant amounts of phosphorus to surface waters. Emissions from industries are driven by the
technology used, the level of wastewater treatment demanded (EC Urban Waste Water Treatment)
82 |
and regulations on discharges (discharge consents) and emissions (UNECE Gothenburg Protocol
to the Convention on the Long Range Transboundary Emissions, EU National Emission Ceiling
Directive and EC Integrated Pollution, Prevention and Control Directive).
Agriculture releases nutrients to the environment through different pathways: emissions of ammonia
to the air and leaching and runoff of nitrogen and phosphorus that reach the river. The export rate
of phosphorus and nitrogen are affected by the amount of fertiliser applied, cultivation practice,
climate, geology, topography, soils hydrology, land management and the spatial location of nutrient
sources in the catchment (Johnes et al., 1996). The transport and power production sectors combust
fossil fuels. By-products of these combustions are nitrogen oxides. Once deposited, they can be
transported to the rivers. 60% of the nitrogen oxides in 1995 came from transport, 21% from the
energy sector and 14% from other industries (European Environment Agency, 1999).
83
agricultural catchments. In the urban/industrial catchments, dilution effects can mean that
nutrients peak at low ows and are potentially nitrogen limited. In agricultural catchments, runoff
can lead to a nutrient peak at high ow with potentially phosphorus limitation (Jarvie et al.,
1998; Mainstone and Parr, 2002). Variation of the ratio between nitrogen and phosphorus in
time also leads to a variation in potential nutrient limitation. However the concentration levels
are also inuenced by plant assimilation and sedimentation (Young et al., 1999).
Phosphorus can be adsorbed or released from sediments. Interactions between river water and
sediments are particularly important for phosphorus (House, 2003). Soluble reactive phosphorus
can be adsorbed or released from sediments as a result of a combination of physico-chemical and
biochemical processes as well as hydrodynamic effects and bioturbation (House and Denison,
1998; House and Warwick, 1999; House, 2003; Jarvie et al., 2005). Particulate phosphorus is
also subject to deposition on the river bed and resuspension according to hydrodynamic factors
and the inuence of biolms in stabilizing the sediment surface (Battin and Sengshmitt, 1999).
The biogeochemical cycling of phosphorus in rivers is therefore complex and inuenced by a wide
range of factors such as the composition and reactivity of the sediments, sediment redox conditions,
growth of biolms, hydrology and antecedent conditions (House, 2003). Nitrogen transformations
include e.g. nitrication of ammonium into nitrate and denitrication of nitrate into atmospheric
nitrogen also depending on the redox potential (Hamilton et al., 2001; Peterson et al., 2001).
Decomposition of organic matter releases plant-available inorganic nutrients to the water
column.
A high population of macrophytes, phytobenthos and phytoplankton can strip soluble reactive
phosphorus (Mainstone and Parr, 2002) and ammonium (Balbi, 2000) out of the water column,
even at high nutrient levels. Effects of nutrients on biota also vary in time: greater impacts by
nutrients during the active season (light and temperature driven) and time to uptake the nutrients
(water residence times, ow driven). Increase in biomass leads to an increase in organic matter.
This organic matter can either decompose in situ (very slow owing rivers) or be carried away,
increasing the nutrient levels of the river either locally or downstream when organic matter is
mineralised.
84
3.2 Macrophytes
Relationships between nutrients and macrophytes
Macrophytes are macroscopic aquatic plants. They are important primary producers in rivers. Their
growth is partly conditioned by the uptake of inorganic nutrients by their roots and their shoots.
Inorganic nutrients can be taken up either from the water column or the sediments, or both in
varying proportion (Clarke and Wharton, 2001). In nutrient-limited rivers enrichment in inorganic
nutrients may lead to an increase in biomass and species richness up to a point when competitive
exclusion occurs (Mesters, 1995).
However, these effects of nutrients are contested in several studies. Demars and Harper (1998)
underlined the difculty of identifying the specic effect of nutrients because of the synergistic
effect of a number of physical factors. Holmes et al. (1999) indicated that species diversity in
itself is not an indicator of trophic status of rivers as a wide range of diversity can occur at any
phosphorus concentration and low to intermediate diversity occur at any phosphorus concentration
as well. The Environment Agency (2002) also pointed out that macrophytes were not an effective
indicator of the level of nutrients in lowland rivers and Madsen and Cedergreen (2002) did not
nd an effect of enrichment on the growth rate of two macrophyte species, suggesting that
nutrients were not limiting for their growth.
Other studies conrmed the prominence of physical characteristics in determining macrophyte
biomass and species composition (Demars and Harper, 1998; Sand-Jensen, 1998; Schorer et al.,
2000; Baattrup-Pedersen et al., 2003; Barendregt and Bio, 2003). They underlined the effects of
ow and its variation, light (water depth, shading by riparian vegetation, suspended solids,
phytoplankton and epiphytes), substrata and weed cutting.
85
+ +
where x7 macrophyte biomass at time t (g C m-2); c10 macrophyte growth rate (day -1); M(T-20)
macrophyte temperature dependency; x12 SRP in pore water at time t (mg P L-1 ); R solar radiation
at time t (normalised to 0-1 from W.m-2); c12 self shading (g C m-2); c11 half saturation of P for
macrophyte growth (mg P L-1); c14 macrophyte death rate (s g C-1 day1); x8 epiphyte biomass at
time t (g C m-2); x1 ow out of reach at time t (m3.s-1);
An example of a macrophyte index used for classication, the Mean Trophic Rank index (Holmes
et al., 1999) is presented in Box 3.1.
The MTR index has been developed for England and Wales to implement the EC Urban Waste
Water Directive. It is used to assess the impact of point sources on rivers (Kelly, 1998). It is based
on the combination of species at a site and, for each species, its indicator value and its abundance.
128 species have been identied for this index. They can be split into 4 broad groups and 10 River
Community Types. These River Community Types are physically described and the mean MTR
86 |
Table 3.1 Summary of some of the relations found between macrophytes and inorganic nutrients.
Biological
element
Total %
SRP
macrophyte
cover
MTR
Soluble NO3
Soluble PO4
Shift in
species
PO43-
Species
richness
NH4-N
PO4-P
Abundance NH4-N
PO4-P
Species
eveness
NH4-N
PO4-P
MTR
NO3-N
NH4-N
N total
SRP
P total
6 phytoNH4-N
sociological NO3-N
groups
PO4-P
Regression:
y = 120.37 + 77.1 . log SRP
(R2 = 0.45. p = 0.002)
Correlation:
0.43 (p < 0.042)
0.58 (p < 0.003)
1st ordination axis correlated
among other things with:
PO43- (R = 0.74, p = 0.0015,
n = 17)
Coefcient of rank
Spearman correlation
0.457 (p < 0.05)
0.611 (p < 0.001)
Coefcient of rank
Spearman correlation
0.600 (p < 0.001)
0.707 (p < 0.001)
Coefcient of rank
Spearman correlation
0.238 (non signicant)
0.780 (p < 0.0001)
Pearson linear correlation
coefcient
0.156
0.299 (p < 0.05)
0.368 (p < 0.05)
0.260
0.294 (p < 0.05)
0.68
+ 0.81 (contextual)
0.92
Sites
Nutrient range
References
River Kennet, UK
n = 20
Not indicated
(Flynn et al.,
2002)
River Welland, UK
Not indicated
(Demars and
Harper, 1998)
28 streams,
The Netherlands
Not indicated
(Mesters, 1995)
(Thiebaut et al.,
2002)
(Thiebaut et al.,
2002)
(Thiebaut et al.,
2002)
Not indicated
(Szoszkiewicz
et al., 2002)
29 sites
(Carbiener
et al., 1990)
value for each of these groups can be used as a reference for physically similar sites. The MTR has
been adapted to several countries, including Poland (Szoszkiewicz et al., 2002).
Other macrophytes indices based on nutrients have been developed in Europe, such as the GIS
Macrophytes in France (Haury et al., 1996), the Trophic Makrophyten Index (Schneider and Melzer,
2003) and the Reference Index (Meilinger et al., 2005) in Germany, and the Canonical-Based
Assessment System for Northern Ireland (Dodkins et al., 2005).
87
Box 3.1 Brief description of Mean Trophic Rank (derived from Holmes et al., 1999).
Interpretation
MTR > 65
25 - 65
MTR < 25
Unlikely to be eutrophic*
Site likely to be either eutrophic or at risk of becoming eutrophic**
Site badly damaged by eutrophication, organic pollution, toxicity or is
physically damaged
*If the score is less than might be expected for a site of this physical type, the site may be at risk of becoming eutrophic.
**If the score is less than might be expected for a site of this physical type, the site is eutrophic or at risk of becoming eutrophic.
3.3 Phytoplankton
Phytoplankton are microscopic plants suspended in the water column. They can include both
true phytoplankton species and phytobenthic species detached by ow, especially after spates
(Descy, 1993; Reynolds, 2003). The generation time of phytoplankton is typically several days.
This makes them highly reactive to changes in the condition of water and light. It also underlines
that a signicant phytoplankton biomass cannot be reached unless the residence time of water in
the river is greater than the generation time (large rivers, slow-moving rivers, canals and on-river
reservoirs).
Nutrient enrichment can lead to an increase in biomass and/or a change in species composition
(e.g. Vanni and Findlay, 1990). Algal blooms have been found to occur principally in spring in rivers
when increasing light and temperature and decreasing ow are favourable to phytoplankton
growth (Marker and Collett, 1997; Balbi, 2000). Species composition is also affected by the way
nutrient enrichment occurs: nutrient pulses allow the persistence of species preferring low and high
nutrient concentrations, thus leading to increased species richness (Hecky and Kilham, 1988).
The effect of nutrient enrichment will, however, be modulated by the initial nutrient concentrations
in the water column. Thus, Mallin et al. (2004) showed no impact of phosphorus enrichment on
phytoplankton biomass (0-5 mg P/l, stream concentration: 3-143 g P/l-1) for 2 streams. In this
study nitrogen enrichment over 200 g N/l in nitrate (stream concentration: 5-930 g N/l-1) led
to an increase in phytoplankton, whatever the form of nitrogen. Young et al. (1999) also showed
that there was little correlation (r = 0.29) between chlorophyll a and phosphorus concentrations
(0.1-6.7 mg PO4-P /l-1) for 3 lowland rivers of the Thames catchment. These studies demonstrate
that the relationships between nutrients and phytoplankton in rivers are not simple.
88 |
Phytoplankton-nutrient relationships
Commonly-used models are mainly simple regression models (Table 3.2). Hakanson et al. (2003)
concluded that it is unlikely that a regression model for mean monthly chlorophyll concentrations
in rivers could yield R2 higher than about 0.6 (for all n). Other more complex and dynamic models
exist and are described in Recknagel et al. (1997).
The dynamic models describe the phytoplankton development and need very substantial data
input e.g. algal growth and respiration rates, light attenuation, nutrient concentrations and
growth rates as a function of the nutrient concentrations. Some of these models are described
below. SWAT2000 (Neitsch et al., 2002): models algal biomass through chlorophyll a, depending
on light, nitrogen and phosphorus. AQUATOX (Park and Clough, 2004): models phytoplankton,
periphyton, macrophytes, invertebrates and sh depending on nutrients, organic matter, organic
toxicant, oxygen, suspended sediments, sediments, temperature and discharges. It is applicable to
streams, lakes and reservoirs.
RIVERSTRAHLER (Billen et al., 1994): combines a hydrological component based on the stream
order and the AQUAPHY model. The AQUAPHY model models the chlorophyll a concentration
and biomass evolution in each stream order depending on light, temperature, ow, ammonium,
nitrate and phosphate concentrations. In Garnier et al. (2002), this model is further rened to
distinguish between diatoms and chlorophycae, to include predation by zooplankton and mussels
and to model the interactions of nutrients across the sediment-water interface.
Table 3.2 Summary of some relations found between phytoplankton and inorganic nutrients.
Biological
element
Sites
Nutrient range
References
Chlorophyll-a,
January to
spring
chlorophyll
maximum
Silicate
NH3
NO3-N
TN
SRP
N/P ratio
Balbi, 2000
Chlorophyll-a, TP
summer
period
Chlorophyll-a NO3
SiO2
Regression
0.71 (p < 0.05)
0.43 (p < 0.05)
0.25 (p < 0.05)
0.20 (p < 0.05)
0.09 (p < 0.05)
0.15 (p < 0.05)
Quadratic model
log(Chl) = 1.65 + 1.99
(log TP) 0.28(log TP)2
(r2 = 0.67)
Chl in mg.m-3 and TP in mg.m-3
89
3.4 Phytobenthos
Whereas phytoplankton is considered to be a good indicator of eutrophication in rivers with a
residence time longer than the generation time of phytoplankton, phytobenthos is a better one
for smaller rivers (Piirso et al., 1997). Phytobenthos is a highly diversied biota (Stevenson, 1996)
with different types of organisms (diatoms, lamentous algae, blue-green etc), growing on different
substrates (rocks, soft riverbed, macrophytes etc) and developing different forms (lamentous,
thin or thick mat etc). Most of the studies undertaken have focused on diatoms. Phytobenthos is
present in every type of river where light reaches the riverbed or surface of macrophytes.
As for all autotrophs, phytobenthos development depends on the availability of inorganic
nutrients. An increase in inorganic nutrients (P and N) potentially leads to an increase in
phytobenthos biomass. Simultaneously, a shift in species composition occurs from slow-growing,
oligotrophic species at very low nutrient concentrations to fast-growing species with competitive
advantages at high nutrient concentrations (Biggs et al., 1998).
The response of phytobenthos to nutrient enrichment depends on whether the nutrient was
limiting and the initial nutrient level. Indeed, Perrin and Richardson (1997) obtained little
phytobenthic response to P addition, a moderate one when adding N, and an even higher one
when adding both N and P (P became limiting once N was added). Stanley et al. (1990)
demonstrated a rapid response of phytobenthic biomass when the P level was initially low (<0.010
mg.l-1) and only a moderate one when ambient P was higher (0.015-0.025 mg.l-1).
Flow and its variation can also play an important role in determining the response of phytobenthos
to nutrient concentrations. The discharge stability over periods of less than a year may govern the
average phytobenthic biomass, and nutrients will control the overall biomass only over prolonged
periods of stability with moderate to low ow (Biggs, 1996). So, a small increase in dissolved
nutrients may greatly increase the frequency of high biomass events if there are infrequent oods
and accrual periods over 100 days (Biggs, 2000).
In term of species richness, nitrogen and phosphorus enrichment have been found to increase the
species richness in oligotrophic streams up to a point where competitive exclusion occurs and
species richness decreases (Marcus, 1980; Snyder et al., 2002). As for phytoplankton (Hecky and
Kiham, 1988), the way nutrients are delivered affects how the community assemblage will
respond. Nutrient pulses can lead to higher richness, with a mix of species of different nutrient
preferences, as found in Finnish rivers (Soininen, 2002).
Kjeldsen (1994) underlined a different response of phytobenthos peak biomass to phosphorus
enrichment depending on the riverbed substrate: on ne-grained sediments phosphorus was the
main driver of the biomass peak, whereas on stony substrate P concentrations are only linked to
the maximum potential biomass and the actual peak biomass is determined by a range of other
factors.
Estimations of biomass levels that hampers the aesthetic quality of rivers have been developed. In
Welch et al. (1988) 100 mg chlorophyll-a per square metre is considered to be the threshold over
which development of phytobenthos, often as lamentous algae, is perceived unfavourably.
Dodds et al. (1998) reviewed several studies of such thresholds. They range from 50 to 200 mg
chlorophyll-a per square metre, and mainly over 100 mg chlorophyll-a per square metre.
90 |
Kiffney and Bull (2000) showed that light was the single best indicator explaining the variation
in peak chlorophyll-a biomass. Light varies seasonally and the quantity that reaches the riverbed
depends on the water depth and a thick carpet of diatoms covering the sediment is often seen
during spring where irradiance is high (Sand-Jensen, 1983). Dense growth of phytobenthos can
cause a high diurnal variations in oxygen concentrations (higher during the day, lower during the
night) unfavourable for other organisms like macroinvertebrates and sh (ten Cate et al., 1991).
Anderson et al. (1999) showed that grazing controlled biomass more than enrichment in soluble
reactive phosphate whereas Walton et al. (1995) pointed out that grazing lead to a shift in
species whatever the enrichment was and grazing is the third dimension in the habitat matrix
developed by Biggs et al. (1998) with an effect similar to spates.
91
Table 3.3 Some examples of relations found between phytbenthos and inorganic nutrients.
Biological
element
SIN
SRP
Sites
Nutrient range
References
33 sites, 13
rivers of Ontario
and Quebec
(Canada)
30 sites, 25
streams,
New Zealand
TP = 6 - 130 g.l-1
TN = 179 - 2873 g.l-1
(Chetelat
et al., 1999)
(Biggs,
2000)
(Biggs,
2000)
SIN
SRP
TN
Spearman correlation:
0.28 (p < 0.01, diatoms at
genus level)
0.42 (p < 0.001, diatoms at
species level)
Spearman correlation:
0.41 (p < 0.01, diatoms at
genus level)
0.45 (p < 0.001, diatoms at
species level)
Pearson correlation coefcient
0.430 (p < 0.001)
% dominance TP
(diatoms)
TDI
NH4-N
Diatom
richness
NH4-N
TP
199 streams,
Not indicated
Mid-Appalachian
streams, USA
(Hill et al.,
2001)
199 streams,
Not indicated
Mid-Appalachian
streams, USA
(Hill et al.,
2001)
9 sites, for
Vistula river,
Poland
11 rivers in
Idaho, USA
(Kwandrans,
2002)
(Snyder
et al., 2002)
92 |
1000
100.0
SIN (mg/m-3)
SIRP (mg/m-3)
Eutrophic
Mesotrophic
Oligotrophic
01
100
0
Days of accrual
A classication of river sites has been developed for the UK based on the Trophic Diatom Index
(TDI) as an indicator of eutrophication (Kelly, 1998). In Italy, the EPI-D is considered suitable to
diagnose inorganic nutrients, organic matter and minerals impacts on phytobenthos (DellUomo
et al., 1999). Lastly, Biggs (2000) developed a classication depending on soluble reactive
phosphorus and soluble inorganic nitrogen, and the number of days of accrual in gravel/cobblebed streams, the boundaries being determined by 2 nuisance levels of chlorophyll a: 60 and 200
mg chlorophyll a per square metre (Figure 3.1).
3.5 Summary
An increase in plant available phosphorus and nitrogen concentrations in rivers potentially leads
to an overall increase in the biomass of phytobenthos, phytoplankton and macrophytes and to
changes in species composition, favouring nutrient tolerant species. Large-scale phytoplankton
growth is generally limited to slow-owing rivers and macrophytes and phytobenthos tend to
occur in rivers where light penetration reaches the river bed.
Nutrient enrichment often leads to an increase in biomass and a change in species from nutrientsensitive toward more nutrient-tolerant species. In term of species richness, enrichment of
oligotrophic streams can lead to an increase in species richness until the enrichment reaches a
threshold after which competitive exclusion of nutrient-sensitive species decreases the overall
species richness. The effects of nutrient enrichment depend on the initial nutrient level. In
oligotrophic streams, even a slight enrichment can lead to a high increase in biomass and alter
the species assemblage, whereas it may not cause any change at higher nutrient levels. However,
no normative thresholds for inorganic nutrients, applicable beyond the individual rivers of the
studies, have been found in the literature.
Inorganic nutrients usually do not directly inuence heterotrophic organisms such as invertebrates
and sh, but it is important to consider also the indirect effects from the changes in the plant
communities when assessing the overall impacts of nutrient in stream ecology. Further, the
autotrophic communities are inuenced by heterotrophic activities (grazing) and the quality of
the river sediment, which must therefore be considered in the assessment of river eutrophication.
93
Numerous studies have been undertaken to examine the relationships between macrophytes and
benthic diatoms and nutrient status in rivers. However, the relationships identied are not
sufciently detailed or targeted to meet the needs in the implementation of the WFD. For setting
the criteria for ecological classication and the environmental objectives, and for planning the
program of measures thereafter, it is necessary to know quantitative relationships between
nutrient concentrations and biological quality elements (periphyton, macrophytes and
phytoplankton) in the different types of rivers. On-going work in REBECCA and other projects such
as DARES (http://craticula.ncl.ac.uk/Dares/index.htm) are exploring these relationships.
Major needs for the implementation of the WFD include clarication of the conditions where the
models and relationships established are operational and valid. The conditions to be claried are
related to the type of river and sediment, the type of vegetation and the concentration level of the
nutrients. Few studies have focussed on the recovery of a river after reduction in either phosphorus
or nitrogen (or both) sources. This aspect should be considered fundamental in determining the
measures needed to be implemented to achieve good chemical and ecological status.
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Journal of the North American Benthological Society 19:32-49
Wright, R.M., and A.J. Mc Donnell. 1986. Macrophyte growth in shallow streams: biomass model. Journal of
Environmental Engineering 112:967-982
Young, K., G.K. Morse, M.D. Scrimshaw, J.H. Kinniburgh, C.L. MacLeod, and J.N. Lester. 1999. The relation
between phosphorus and eutrophication in the Thames catchment, UK. Science of the Total Environment
228:157-183
Zelinka, M., and P. Marvan 1961. Zur Przisierung der biologischen Klassikation des Rheinheit Fliessender
Gewsser. Archiv fur Hydrobiologie 57:389-407
99
4.1 Introduction
The European Environment Agency (EEA), in the Dobris Report and in the Report on European
Rivers and Lakes (EEA 1991, 1994), underlined the importance of organic pollution in European
rivers. Although, more recently, the EEA has stated (EEA, 2003a and 2003b) that the amount of
degradable organic matter (OM) discharged with wastewaters has been signicantly reduced in
Europe since the 1990s. The objective of this chapter is to review the existing knowledge on the
relationships between the content of organic matter in rivers and the WFD relevant biological
quality elements, mainly focusing on the impacts of OM discharged with wastewaters, one of the
main causes of pollution in rivers.
Distance
High Respiration
100
The major sources of organic matter pollution are domestic wastewater, industrial wastewater
from the food, pulp and paper processing industries and agricultural discharges from livestock
production and sh farming. In addition, occasional discharges, such as storm-water run-off from
urban areas, can also be important sources of pollution.
The specic impacts mainly depend on two factors: the amount and the quality of the organic
matter discharged. Furthermore, the extent of the ecological damage depends on the
hydromorphological characteristics of the river and the presence of other concurrent pressures
affecting the system. Figure 4.2 shows changes in water quality and biota downstream of
wastewater discharges. It is worth noting that the benthic fauna can be more heavily affected in
areas next to the discharge point, rather than at sites where oxygen is at it its lowest, due to
deposits of organic matter or bacterial growths on the riverbed. These patterns are typical for
large rivers while in small streams chemical and biological characteristics downstream of a
wastewater input show a much higher variability.
Outfall
BOD
Oxygen
NH4
NO3
PO4
Sewage fungus
Bacteria
Algae
Tubicidae
Clean water fauna
Chironomidae
Distance downstream
Asellus
101
Decomposition and dilution processes reduce the concentration of organic matter downstream of
the discharge point and, as the distance from a sewage efuent increases, organic matter
concentration may possibly reach the same values detected immediately upstream of the discharge
point. The rst models (Streeter and Phelps, 1925) were based on oxygen consumption described
by a rst order mineralisation of the organic matter and a re-aeration proportional to the oxygen
decit. The implementation of this model during the last decades has led to the development of
more comprehensive models describing the temporal and spatial dynamics of the oxygen
concentrations in rivers. Examples of such models are the river models established by the IWA
(International Water Association) Task Group on River Water Quality Modelling (Reichert et al.,
2001; Shanahan et al., 2001; Vanrolleghem et al., 2001) and the modelling framework for
simulation of river and stream water quality available at US EPA homepage (Chapra and Pelletier,
2003). These recent river water quality models give a dynamic description of chemical variables
such as dissolved oxygen (DO, mg O2 /l), biological oxygen demand (BOD) and ammonium.
Domestic and industrial wastewater discharges are the most important sources of organic
pollution in rivers (Table 4.1). If not properly treated, such discharges greatly affect the quantity
and quality of organic matter in rivers. Since organic matter represents a trophic resource for many
organisms, these changes will directly affect the river biota.
Table 4.1 Concentration (mg/l) of various compounds in wastewaters.
Parameter
Suspended Solids
BOD5
COD
N total
N organic
N-NH4
P total
Proteins
Fats
Carbohydrates
Food processing
(IRSA, 1980)
Urban Runoff
(Gray, 1989)
Paper industry*
Domestic
(Henze et al., 1995)
4.2-13000
5.2-25000
2-22400
0.05-1313
0.3-510
0.1-66
0.02-520
210-560
1.2-3000
100-1500
2-11300
1-700
5-3100
1.1-6.2
0.1 16
0.1-14
0.09-4.4
<5-70
90-1150
235-2000
3.2-51.2
0.1-0.3
120-450
100-350
210-740
20-80
8-30
12-50
4-23
7-25
30-100
10-40
102
The parameters generally used to describe the levels of organic pollution in both wastewater and
rivers are:
Biological Oxygen Demand (BOD, mg O2 /l). The BOD-analysis is performed by measuring the
oxygen consumption (by micro-organisms) for the oxidation of organic matter and ammonia
in a sample during a predetermined period (5, 7 or 25 days). The method consists of lling to
overowing, an airtight sample-bottle of the specied size and incubating it at 20C in the
dark to prevent any possibility of photosynthetic production of DO. Dissolved Oxygen is
measured initially and after incubation, and BOD is computed from the difference between
initial and nal DO (APHA, 1998). The addition of thiourea to the sample prevents the
oxidation of ammonia, thus making possible to measure BOD due to organic matter only.
Chemical Oxygen Demand (COD, mg O2 /l). The COD analysis is performed by a chemical
oxidation with dichromate or permanganate. COD-values determined by oxidation with
dichromate give a good picture of the total content of organic matter in the sample as almost
all organic matter is oxidised, while permanganate gives an incomplete oxidation.
Total Oxygen Demand (TOD, mg O2 /l). The TOD analysis is performed by oxidation at high
temperature in the presence of a suitable catalyst. All organic compounds are oxidised by
TOD analysis.
Total, particulate and dissolved organic matter (TOM, POM and DOM, mg/l). The separation
between dissolved and particulate matter is traditionally achieved by ltering through 0.2-0.7 m
lters. These different fractions are generally determined by instrumental analysis and expressed
as total, particulate and dissolved organic carbon (TOC, POC and DOC, mg C/l). Carbon is
approximately 50% of the organic fraction in domestic wastewaters (Tchobanoglous et al., 2002).
103
Typical BOD levels in untreated and standard biologically treated urban wastewater are given in
Table 4.3. An extended biological treatment is likely to produce a wastewater with a BOD5 of
about 5 mg/l which is far below the limits of 20 mg BOD/l and 75 mg COD/l required by the
Urban Waste Water Directive (91/271/EEC).
Table 4.3 Values for the different measuring methods for two different types of wastewater (Henze et al., 1995).
Element
CBOD5
CBOD7
CBOD
CCOD
SS,COD
XS,COD
Name
Raw Wastewater
(g O2 /m3)
280
320
400
600
60
200
25
30
35
100
5
10
104
Degradation of organic matter by heterotrophic bacteria is one of the major processes controlling
the oxygen level of aquatic ecosystems and thus their quality. However, parameters that have
been traditionally used in models for describing organic matter degradation, such as BOD, COD
and TOC, are often insufcient to predict correctly the impact of waste water release on aquatic
ecosystems. Ecological models able to describe riverine ecological processes and useful for the
development of rehabilitation scenarios would require a detailed characterization of the quality
of the organic matter (biodegradable and refractory; Servais et al., 1999) and a better
understanding of the complex relationship between the bacterial community (structure and
functioning) and organic matter availability (Fazi et al., 2005).
105
Table 4.5 Saprobic classes related to BOD5 (mg/l), DO (mg/l) and NH4+ (mg/l) values.
Saprobic classes
Saprobic index
BOD5 (mg/l)
DO (mg/l)
NH4+ (mg/l)
<0,5
<1,5
<2,5
<3,5
<4,5
<1
<2,5
<5
<10
<50
>8
>6
>4
>2
>0,1
<0.5
<0.9
<1.7
<3.3
<5.9
Xenosaprobity
Oligosaprobity
-mesosaprobity
-mesosaprobity
Polysaprobity
Degree of pollution
IV
Moderate ow
Slow ow
Good ow
III
II
I
0
10
12
BOD5 (mg/l)
14
16
18
20
Figure 4.3 Relationships between the degree of pollution (saprobic index) and the concentration of
degradable organic matter (BOD5) in Danish streams (Andersen, 1994).
22
106
4.4 Phytobenthos
Attached lamentous green algae such as Cladophora are a frequent nuisance in shallow rivers
polluted by wastewaters. Usually their occurrence is mainly linked to the level of inorganic
nutrients in the river water (Whitton, 1970), but often enhanced growth is not seen in rivers with
elevated nitrate and phosphate concentrations if otherwise unpolluted. Other factors such as
organic compounds can be important.
Benthic diatoms are widely used as water quality indicators in rivers. In particular, diatom species
composition is used to evaluate water quality in terms of organic pollution (Fabri and Leclercq,
1984; Sldec ek, 1986; Descy and Coste, 1991). Most of the diatom indices, e.g., the Trophic
Diatom Indices of Hofmann (1994) and Kelly (1998), the saprobic index of Sldec ek (1973), the
Pollution Index of Descy (1979), and the Generic Diatom Index (Coste and Aypassorho, 1991),
are in essence numerical models that use species indicator values to predict water quality
parameters (Potapova et al., 2004).
^
Occurrence, species composition and biomass are usually related to the level of inorganic nutrients.
Organic pollution also affects the occurrence of benthic diatoms, and for many species saprobic
values can be found in the literature (Liebmann, 1951). Eichenberger and Wuhrmann (1966)
studied the effects of addition of sewage to experimental channels in Switzerland and found
signicant impacts on autotrophic and heterotrophic microbenthos with organic enrichments
corresponding to a few mg BOD/l.
4.6 Macroinvertebrates
Currently, macroinvertebrates are the most commonly used element for biological classication of
rivers in Europe. Although the details in methodologies might vary from country to country, the
use of macroinvertebrates to assess the effects of organic pollution of rivers has a long history
throughout Europe. Since the key products of organic matter decomposition are nutrients,
eutrophication is very closely linked to organic pollution. Effects of organic pollution and
eutrophication on stream benthic fauna are linked to each other by the processes of organic
matter and nutrient transformation.
107
The rst biotic index based on macroinvertebrates was the Trent Index developed by the Trent
River Authority (Metcalfe-Smith, 1996). In common with the Saprobic System, the Trent Index
mainly targeted organic pollution. The Trent Index has been the forerunner to all biotic indices
currently in use in Europe. They differ, however, due to the regional differences in macroinvertebrate
species composition in Europe and due to the introduction of various modications related to the
taxonomic level used, the method of index calculation etc.
Currently used macroinvertebrates methods and metrics include:
ASPT, Average Score per Taxon used in the UK (Armitage et al., 1983)
BMWP, Biological Monitoring Working Party Score used in the UK (Armitage et al., 1983) and
Spain (BMWP, Alba-Tercedor and Sanchez-Ortega, 1988)
BBI Belgian Biotic Index (De Pauw and Van Hooren, 1983)
DSFI, Danish Stream Fauna Index (Skriver et al., 2000)
EPT index, number of Ephemeroptera, Plecoptera and Trichoptera taxa usually employed to
derive additional information, not to directly classify river sites
IBE (Indice Biotico Esteso), Italian Extended Biotic Index (Ghetti, 1997; APAT/IRSA-CNR,
2004), is a modied version of the Extended Biotic Index (Woodiwiss, 1964)
IBGN, Indice Biologique Global Normalis (AFNOR, 1992).
The recent EU project The Development and Testing of an Integrated Assessment System for the
Ecological Quality of Streams and Rivers throughout Europe using Benthic Macroinvertebrates
(AQEM) developed alternative approaches to assess the impact of organic pollution by dening
type-specic multimetric indices (Hering et al., 2003, 2004). Many different metrics were tested
and multimetric indices and/or scoring systems were developed for individual stream types and
countries. The majority of these scoring systems show a good relationship with the magnitude of
organic pollution within each stream type (e.g. Buffagni et al., 2004; Pinto et al., 2004; Skoulikidis
et al., 2004). These results highlight the need for an intercalibration of the biological response to
organic pollution across Europe (Sandin and Hering, 2004).
The current river monitoring procedures and assessment methods should be improved to cover
different habitat types in rivers. The results of the AQEM project concerning differences between
depositional and transport reaches of rivers (i.e. pools versus rifes), indicate that habitat type
should be considered (Brabec et al., 2004; Buffagni et al., 2004; Morais et al., 2004).
Examples of the relationship between single biological metrics, multi-metric indices and abiotic
indicators of organic pollution are shown in Figure 4.4. The relationships are based on the data
presented by Buffagni et al. (2004), which refer to small-sized rivers in Southern Italy. Rivers in
this geographic area suffer from a multi-pressure situation but are mainly affected by organic
pollution. A multivariate axis (PCA) based on BOD5, NH3, NO2, PO4, Escherichia coli, Cl- and O2
concentration values, which are all tracers of organic pollution, was derived for samples from three
sampling seasons. The obtained PCA axis was related to the number of Trichoptera families (Figure
4.4: top, left), one of the single metrics that performed best in demonstrating organic pollution
(Pearson R2=0.587).
108
10
8
1.0
R (Pearson) = 0.587
2
ICM index
#Tricoptera families
12
6
4
1.0
-1.0
0.0
1.0
Organic pollution score (PCA)
R2 (Pearson) = 0.510
0.2
2.0
2.0
1.0
0.0
1.0
Organic pollution score (PCA)
1.0
R2 (Pearson) = 0.650
ICM index
MMI index
0.8
0.6
0.4
0.2
2.0
0.6
0.4
2
0
-2.0
0.8
2.0
R2 (Pearson) = 0.307
0.8
0.6
0.4
1.0
0.0
1.0
Organic pollution score (PCA)
2.0
0.2
0.0
2.0
4.0
6.0
8.0
BOD5 (mgl-1)
10.0
12.0
Figure 4.4 Examples of biological response to organic pollution in small-sized Southern European rivers
(data from Buffagni et al., 2004). From top to bottom and from left to right, the relationship between
Number of Trichoptera families, ICMi and a Multi Metric Index to a multi-variate axis (PCA) of organic
pollution is shown. The fourth diagram illustrates the relation between the ICM index and BOD5 values.
The combination of single metrics into multimetric indices usually enhances the general
performance of the index. In the example, the Intercalibration Common Metric index (ICMi:
Buffagni et al., 2005) developed for the European Intercalibration process and based on a family
level identication, is related to the multivariate axis of organic pollution. Along the x axis, high
values reect conditions of strong organic pollution.
Although the R2 value slightly decreases, the overall response of the index is more suitable for
describing organic pollution (with the exclusion of heavily polluted sites). The performance of the
Multi-Metric Index dedicated to this stream type (left, bottom) is the best among all the metrics
tested (Pearson R2 = 0.650). Nevertheless, a certain degree of dispersion of samples around the
regression line can be seen. This is not surprising, because the index is designed to assess general
degradation of river sites (i.e. not only organic pollution; Buffagni et al., 2004). This underlines
the need for considering organic pollution indicators together with e.g. hydro-morphological and
toxic parameters, so that a multi-pressure impact can be properly interpreted. The last graph
(right, bottom), shows the relationship between ICMi and a single organic pollution descriptor
(BOD5), which indicates that attempts to nd simple direct relationships betweem biological and
chemical metrics can fail or yield poor results when analysing eld data.
109
9 (100%)
Cyprinid waters
8 (50%)
5(100%)
7 (50%)
BOD5
mg/l
Mandatory Guidance
Total ammonium
mg/l
Mandatory Guidance
Free ammonia
mg/l
Mandatory Guidance
0.04
0.025
0.005
0.2
0.025
0.005
4.8 Summary
River ecosystems experience many different types of organic inputs. While, in Europe, wastewater
discharges from urban areas and industry have substantially declined during recent decades,
other sources have become more important. These include urban storm-water, discharges from
agricultural husbandry, sh-farming, wastewater from scattered dwellings, and organic inputs
from eutrophied lakes.
There is substantial evidence in the scientic literature that benthic macroinvertebrates, benthic
algae and sh are effective biological elements for the assessment of the impact of organic matter
on river ecosystems. In the past, the relationships between BOD levels and saprobic indices have
been well described, especially for rivers polluted by untreated wastewaters. However, organic
110
pollution impacts are not necessary only related to oxygen decits. Changes in biota also occur at
low increases in organic matter (OM) concentration and without a substantial decit of oxygen in
the water column. Likewise, the quality of the organic matter discharged seems to be another
important characteristic in determining the impact on river biota. The chemical structure of
organic compounds inuences the behaviour of OM in aquatic ecosystems affecting its biological
persistence, microbial communities, interaction with suspended minerals, properties in the
production of colloids and gels and its complexing ability towards heavy metals, etc. All these
effects should be further investigated.
Mathematical models are available for the evaluation of chemical water quality. Concentrations
of DO, BOD, ammonium and other chemical constituents are well described in rivers as a function
of discharged organic pollutants. Nevertheless these models usually require rates and kinetic
coefcients not always available at local scale for different river types. Moreover, modes and
resilience time for river ecosystems recovering from organic pollution are not yet fully understood.
Despite the overwhelming scientic knowledge on the biological impacts of organic pollution in
river ecosystems, there is still a lack of operational tools to estimate the amount of OM to be
reduced in order to meet biological quality criteria for different river types in Europe.
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Acidication
117
5.1 Introduction
Acidication of water implies a pH reduction. The pH reduction can be due to anthropogenic
activities (e.g. burning of fossil fuels) but also to natural processes (e.g. presence of organic acids).
It is important to separate these two causes of low pH as the ecological impact of elevated H+ will
vary. This difference is to a large extent due to the interaction between acid rain and the
mobilisation of aluminum (Al). Al interacts with metal sensitive tissues such as the gills of sh and
invertebrates and will impair physiological processes in both plants and animals affecting growth
and reproduction (Gensemer and Playle, 1999). While low pH will aggravate the effects of Al,
increased concentrations of e.g. calcium (Ca), increased ionic strength and the presence of various
organic and inorganic ligands will act to reduce toxicity (see reviews in: Rosseland and Staurnes,
1994; Gensemer and Playle, 1999). The ecological effect depends on exposure intensity, the
species and life stages exposed, exposure duration and the possibility for post-exposure recovery
of a sub-lethal exposure. As toxicity is related to both H+ and Al, acidication is a combined
stressor. The two toxicants must be interpreted in combination, but also separately. While some
species are mainly H+-sensitive, others are mainly Al-sensitive (Gensemer and Playle, 1999).
The ecological effect depends as such on the relative contribution of the prime toxicants and how
these act in concert. Due to the combined action of H+ and Al, the pH-limits restricting organisms
in naturally acidic water-bodies are normally lower than the limits restricting the same species in
water having elevated concentrations of Al. pH limits restricting organisms are further inuenced
by all confounding factors giving rise to a large variability in the response surfaces.
The most obvious biological impacts of acidication are related to changes in the composition
and abundance of invertebrate and macrophyte periphyton communities and the reduction or
extinction of sh populations (Raddum and Fjellheim, 1984; Farmer, 1990; Rosseland and
Staurnes, 1994; Gensemer and Playle, 1999). The community structure changes from one
supporting acid sensitive organisms to one supporting acid tolerant organisms. Only few of these
changes are acidication specic, as similar changes can be related to a variety of pressures.
Annex V of the WFD outlines both the physico-chemical and biological elements to be included. The
chemical elements are pH, alkalinity and acid neutralising capacity. All three are related to the true
toxic components: hydrogen activity and Al. The annex does not detail how naturally acidic sites
should be separated from sites being acidic due to anthropogenic activity. The biological elements:
macrophytes and phytobenthos, phytoplankton, benthic invertebrates and sh are largely assessed
using species composition and abundance with the addition of age structure for sh.
118 |
only local effects, while acid rain, being trans-boundary, has regional and global effects. Acid rain
mainly results from the burning of fossil fuels and the subsequent emission of sulphur dioxide and
nitrogen oxides into the atmosphere. In addition, ammonia from agricultural activities contributes
locally to acid loading through the nitrication process. In air and in contact with water the oxides
are transformed into sulphuric and nitric acids. These acids can be transported over large distances,
before being deposited as acid rain. In Europe, acidication has a negative impact in water
bodies with a low alkalinity, i.e. in non-calcareous catchments.
The cause and effect chains linking acid rain to acid water were rst established in the 1950s.
Acidication became an international issue around 1970 (Almer, 1974). Since then, focus has
changed from pH being regarded as the main factor for environmental change prior to 1980 to
include the toxicity of Al mobilised at low pH values. Focus has also changed from proving effects
and establishing causal relationships in the 1980s to the present day focus on recovery or the lack
of recovery following deposition reductions (Skjelkvle et al., 2003). Although water quality has
improved, episodes can still be detrimental and hinder the reestablishment of acid sensitive species.
In addition, recolonisation rates are low in regions heavily impacted by acid rain.
Owing to the reduced emission of sulphuric compounds in Europe there has been a substantial
reduction in the atmospheric deposition of acidity since the 1970s. However, there has been no
signicant decrease in nitrogen deposition (Alewell et al., 2001). These trends are visible in the
changes in wet deposition of sulphur and nitrogen over southern Norway (Figure 5.1). Future
effects relating to the deposition of N represent an uncertainty. The reduction in acid loading will
initiate a recovery process, the rate of which is related to changes in the deposition of acids, but
also to local variations in soil properties e.g. weathering rates (Skjelkvle and Wright, 1991). Future
changes in water quality will also depend on climate change, where sea-salt episodes, elevated
temperature and the mobilisation of organic matter will all contribute to changes in acidication.
Wet deposition mg/m2
1500
1000
500
SO4-S
NO3-N & NH4-N
0
1974
1982
1990
Figure 5.1 Trends in the wet deposition of sulphur and nitrogen compounds shown as averages from
7 representative sites in southern Norway.
2002
119
120 |
350
7.5
6.5
250
300
pH
6
5.5
5
4.5
5 0
50
100
200
150
100
50
4
100
0
100
150
5 0
ANC-1 (CB)
50
100
150
ANC-1 (CB)
Figure 5.2 Relationships between pH (a) and labile aluminium (b) and ANC (base cations - anions)
for Norwegian lakes having low (<1.5 mg C/l) and high (>5 mg C/l) organic content (Data from the
Norwegian 1000-lakes survey in 1986).
probability of occurrence
1.0
1.0 B
0.8
0.8
0.6
0.6
0.4
0.4
0.2
0.2
0.0
0.0
1.0
100
50
100
150 200
ANC (eq/l)
0.8
1.0
probability
0.6
0.4
0.2
0.0
100
50
50
50
ANC (eq/l)
100
150
200
0.8
0.5
extinct
reduced
0.3
not affected
0.0
80 70 60 50 40 30 20 10 0 10 20 30 40
ANC (eq/l)
Figure 5.3 Response curves showing the relationship between ANC and the probability of occurrence
of (A) the diatom Achnanthes minutissima, (B) the mayy Baetis rhodani and (C) non-impoverished
macroinvertebrate assemblage and (D) brown trout. Figures redrawn from Juggins et al. (1995) and Lien
et al. (1996).
121
Due to the combined action from H+ and LAl, it is important not to confuse natural acidic
conditions with anthropogenic acidication. While both are associated with a low pH, elevated
levels of Al in its toxic form are mainly found as a result of anthropogenic acidication. Water
bodies acidied by natural processes can have a low pH due to a high content of organic (humic)
matter and following oxidation of sulphide rich soils. Naturally acidic water bodies can as such
have a high ecological status despite having a low pH restricting the diversity of the biological
community.
eq/ha/yr
<200
200-400
400-700
700-1000
1000-1500
>1500
http://www.acidrain.org/acidication.htm
122 |
Geochemistry and soils play a central role in the response of forests, lakes and rivers to acid rain.
Dynamic, process-based models integrate and interpret theoretical knowledge from soil science
and hydrochemistry with results from experiments and monitoring. Response times are related to
factors such as mineral and organic matter content, weathering rates etc; all properties that are
more or less unique for an individual site. Because of the complex nature of interactions, dynamic
models are used to predict the rate of change over time. Experimental data from ongoing
experiments (long time-series) are used to validate these models. The main dynamic model used
in acidication studies is the MAGIC model.
At present there are no dynamic models for biological responses to acidication except for a
model developed for Atlantic salmon in Canada (Korman et al., 1994). There are several nondynamic models based on the relationship between species composition and abundance and
water chemistry (see chapter on individual organism groups).
100
% total CO2
CO3- -
HCO3-
Free CO2
50
0
4
10
11
12
pH
Figure 5.5 Relation between pH and the relative proportions of inorganic carbon species of CO2 (+H2CO3),
HCO3- and CO3- -. Slightly modied from Wetzel (1983).
123
Total number of
taxa assessed
Acid tolerant
pH < 5
Moderately sensitive
pH > 5.5-6.0
Strongly sensitive
pH > 6.5
127
70
11
208
34
12
5
51
8
9
3
20
36 (divided in 2 groups)
28
3
67
49
29
Not assessed
78
124 |
Cyanobacateria
<5
5-5.5 5.5-6
Tolerant
Slightly sensitive
Moderatly sensitive
Sensitive
Very sensitive
6-6.5 6.5-7
7-7.5 >7.5
Chlorophyta
<5
5-5.5 5.5-6
6-6.5 6.5-7
7-7.5 >7.5
Critical limits
Lindstrm et al. (2004) showed the relationship between an index based on the presence of acidsensitive attached algae (Index of Acid Sensitivity) and the pH values of Norwegian rivers (Figure 5.7).
They concluded that the index showed that a pH > 6.3 was needed to ensure that the algal
community was not impacted by acidication. They also concluded that the algal community had
a substantial probability of being impacted if the pH was less than 5.6. In reference lakes that
have a naturally low pH, the community structure resembles that of an acidied lake.
The variability observed within the pH range 5.6 to 6.3 could have been caused by episodes, but
could also have been due to toxic properties of Al being present in anthropogenically acidied
water, but absent in waters having a naturally low pH (Gensemer and Playle, 1999).
125
n = 365
14
12
IAS
10
8
6
4
2
0
4.5
5.5
pH
6.5
7.5
126 |
http://www.aqem.de.
127
and 5.5, a pH interval that has not received much attention in the Nordic indices (Guerold et al.,
1999). While these various indices give good predictions on a local scale, they are inadequate to
predict subtle, but ecologically important changes on a regional scale.
Humic substances
In general, data from the Nordic countries indicate a higher tolerance to low pH at high levels of
TOC (total organic carbon). It is generally assumed that humic substances detoxify the water
making metals and in particular Al less bio-available. It has been shown experimentally that humic
substances may reduce the toxic effect of low pH on the mayy Baetis rhodani and the crustacean
Gammarus lacustris (Bkken and Aanes, 1990). Using pH as the indicator avoids some of the
difculties in interpretation as discussed for the relationship between ANCcb, pH and LAl.
128 |
As
Cd
Cu
Pb
Hg
Ni
Zn
0.001 0.01
0.1
1
10
Concentration mg/L
100
5.6 Fish
Fish are generally more sensitive to Al than to the pH reduction per se. For example, while Atlantic
salmon are unaffected by H+ concentration down to pH values lower than 5.4 (Lacroix and
Townsend, 1987; Fivelstad et al., 2004), in the presence of bio-available Al the species is extinct
in rivers having average pH values lower than 5.5 while its abundance is reduced when the pH is
lower than 5.9. Many of the currently acidied rivers have a background (historic) pH level that
today would indicate toxic conditions. Based on such observations, it is concluded that pH alone
does not give a satisfactory prediction of sh population status (Kroglund et al., 2002). Therefore,
understanding the interaction between pH and Al, but also between Al and sh and Al and other
water quality constituents is fundamental to the understanding of the mechanisms controlling
population changes.
Sensitivity to acidication varies between species, life stages and strains. Where Atlantic salmon
(Salmo salar), brown trout (Salmo trutta), roach (Rutilus rutilus) and Arctic char (Salvelinus
alpinus) are more sensitive than perch (Perca uviatilis). While acid-sensitive sh species have
declined the most, even populations of more acid-tolerant species are affected in some regions of
Europe (Rask and Tuunainen, 1990; Rask et al., 1995). Within Europe, the number of populations
affected runs into thousands. In addition, an even higher number of populations have suffered
reduced viability, i.e. show a non-healthy status. Compared to the number of lakes that have lost
their sh populations, sh kills are rare. In most lakes and rivers, the effects of acidication are
129
only observed as changes in sh species composition and/or abundance (Rask and Tuunainen,
1990; Hesthagen et al., 1999; Tammi et al., 2003). The fact that sh kills are rare events, despite
populations being lost, suggests that density reductions occurs at life stages where kills are not
easily observed (e.g. egg and fry) and that density reduction is a gradual event (e.g. more related
to sh health and susceptibility to diseases, predation etc) rather than an acute event. Fish kills
have been observed under extreme conditions and examples of total sh loss have been recorded
in Norway, Scotland and Wales (Hindar et al., 1994). Fish kills (Salmo salar) were observed in
several Norwegian rivers in the years between 1910 and 1920, kills that were most likely due to
acidication and sea salt episodes (Hindar et al., 1994; 2004). Despite massive sh kills, it took
more than 40 years for the various affected populations to go extinct. This illustrates that linking
dose to response is not necessarily a straightforward process.
The alteration or loss of sh populations is not caused by food shortage. Bottom-up relationships
are therefore only of minor importance in acidied systems (Rosseland and Staurnes, 1994;
Gensemer and Playle, 1999). Fish population health is mainly related to Al, where the activity of
H+ will enhance toxicity. Since Al is not vital to any aquatic biota, the species have not evolved
any defense mechanism specic for this metal. Al exercises its toxic properties by being accumulated
onto the sh gill affecting both tissue function and properties (Rosseland et al., 1994; Gensemer
and Playle, 1999). The accumulation is directly related to the concentration of in situ fractionated
Al (Gensemer and Playle, 1999). The relationships are poor when based on water samples where
the dynamic nature of Al has been stabilised through ageing (Kroglund et al., 2001). Al is
accumulated onto the mucus layer surrounding the gill, onto cell walls and is over time transported
inside the cell. The toxic role and effect depends on the concentration, exposure duration and the
location where the Al is accumulated. As the speciation and hence toxicity of Al is dynamic, Al
does not t directly into biotic ligand models as these assume that the metals are present in a
free, and stable form (Chapman et al., 2003). Al characteristics are more dynamic in rivers than
in lakes, and more at pH levels around 5.6 to 6.2 than at pH levels lower than 5.2. The probability
for errors is as such related to pH and to water retention time.
The most exhaustive studies have been performed on salmonids. A water quality that has no
appreciable effect on Atlantic salmon fry and smolt production can still have a large effect on the
seawater survival of the postsmolt. Concentrations of LAl that are below the analytical certainty
can impair enzyme activities essential for hypoosmoregulation (Kroglund and Finstad, 2003). Due
to this analytical uncertainty, salmon health is best related to Al accumulated onto the gills. The
present day reduction in Atlantic salmon catches across Europe and the North Atlantic could
therefore be due to acidication related causes in addition to other pressures.
5.7 Summary
Acidication is caused by atmospheric deposition of nitrogen and sulphur compounds which
reduces the pH in water bodies with low alkalinity. Reducing the pH has an impact on the chemical
water quality through increasing concentrations of toxic Al and heavy metal species as well as
changing the CO2-bicarbonate equilibrium. A high nitrogen deposition can alter the nutrient
balance of freshwaters (e.g. N:P ratio).
130 |
The biological impacts have been demonstrated for sh, invertebrates and plants in rivers and
lakes. The impact increases when pH is lowered below 6.5. The specic impacts also depend on
the concentration of aluminium and total organic carbon (TOC or humus). Naturally acidic water
bodies generally have a more diverse ora and fauna compared to anthropogenically acidied
water bodies with the same pH level.
There are still several major knowledge gaps that need to be lled for successful implementation of
the WFD. Further work is needed on the relationship between atmospheric loading and the resulting
chemical water quality in different types of catchments. It is necessary to develop quantitative metrics
for biotic elements in water bodies susceptible to acidication, and to describe ecosystem effects of
reductions in acid precipitation. Chemical and biological indices must be harmonised. Models currently
in use are awed with respect to their ability to identify dose-response relationships.
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Raddum, G.G. and B.L. Skjelkvle. 1995. Critical limits of acidication to invertebrates in different regions of
Europe. Water Air and Soil Pollution 85:475-480
Rask, M. and P. Tuunainen 1990. Acid-induced changes in sh populations of small Finnish lakes. In: Kauppi
P., P. Anttila and K. Kenttmies (Eds.), Acidication in Finland, Springer-Verlag, Berlin, pp. 911-927
Rask, M., Mannio, J., Forsius, M., Posch, M. and Vuorinen, P. 1995. How many sh populations are affected
by acid precipitation? Environmental Biology of Fishes 42:51-63
Redeld, A.C., 1958. The biological control of chemical factors in the environment. American Scientist
46:205-222
Reuss, J.O. and D.W. Johnson. 1986. Acid deposition and the acidication of soils and waters. Ecological
Studies. Springer Verlag, New York pp. 119
Riis, T. and K. Sand-Jensen. 1998. Development of vegetation and environmental conditions in an oligotrophic
Danish lake over 40 years. Freshwater Biology 40:123-134
Roelofs, J.G.M. 1983. Impact of acidication and eutrophication on macrophyte communities in soft waters
in the Netherlands.1: eld observations. Aquatic Botany 17:139-155
Roelofs, J.G.M., E. Brouwer, R. Bobbink. 2002. Restoration of aquatic macrophyte vegetation in acidied and
eutrophicated shallow soft water wetlands in the Netherlands. Hydrobiologia 478:171-180
Rosseland, B.O. and M. Staurnes. 1994. Physiological mechanisms for toxic effects and resistance to acidic
water: an ecophysiological and ecotoxicological approach. In: Steinberg, E.W. and R.F. Wright (Eds.),
Acidication of freshwater ecosystems: implications for the future. John Wiley & Sons. pp. 228-246
Sand-Jensen, K., M. Sondergaard. 1979. Distribution and quantitative development of aquatic macrophytes
in relation to sediment characteristics in oligotrophic Lake Kalgaard, Denmark. Freshwater Biology 9:1-11
Skjelkvle, B.L. and R.F. Wright. 1991. Overview of areas sensitive to acidication in Europe. Oslo:Norwegian
Institute for Water Research. 24/1990, 1991
Skjelkvle, B.L., C. Evans, T. Larsen, A. Hindar and G.G. Raddum. 2003. Recovery from acidication in
European surface waters: a view to the future. Ambio 32:170-175
Smolders, A.J.P., E. Lucassen, J.G.M. Roelofs. 2002. The isoetid environment: biogeochemistry and threats.
Aquatic Botany 73:325350
Tammi, J., M. Appelberg, U. Beier, T. Hesthagen, A. Lappalainen and M. Rask. 2003. Fish status survey of
Nordic lakes: effects of acidication, eutrophication and stocking activity on present sh species composition.
Ambio 32:98-105
Turnbull, D., C. Soulsby, S. Langan, R. Owen, and D. Hirst. 1995. Macroinvertebrate status in relation to
critical loads for freshwater: a case study from NE Scotland. Water, Air and Soil Pollution 85: 2461-2466
Vestergaard, O. and K. Sand-Jensen. 2000. Aquatic macrophyte richness in Danish lakes in relation to
alkalinity, transparency and lake area. Canadian Journal of Fisheries and Aquatic Science 57:2022-2031
Warfvinge, P., S. Lofgren and U. Lundstrom.1995. Implications of natural acidication for mitigation strategies
in northern Sweden. Water, Air and Soil Pollution 85: 499-504
Wetzel, R.G. 1983. Limnology. Second edition. Saunders College Publishing, New York. pp. 767
Hydromorphological
pressures
135
6.1 Introduction
Hydromorphological pressures in lakes are related to the human need to control the water levels
of lakes for various reasons such as production of hydropower, ood prevention, recreation,
navigation, and supply of water for agricultural or human consumption. Regulation practices vary
and depend on the objectives of regulation. In a typical hydropower regulation project in the
northern hemisphere, water level during the summer period is increased, relative to the unregulated
regime, and during the winter period, when the demand for and the price of electricity is highest,
the water level is strongly lowered. Flood prevention regulation follows a similar pattern during
the winter, but in summer some storage capacity is left to allow for ash ood events. When the
major objective of the regulation is recreation or navigation, then regulated water levels are often
more stable than natural ones. If the water level is regulated for water supply use, the water level
uctuation is more irregular and depends on the specic use of raw water.
Although hydromorphological pressures are specic to particular water bodies and their regulation
regime, some generalizations can be made. Hydropower effects are typical in northern and high
altitude lakes, which usually are not impacted by other pressures, whereas pressures due to
regulation for navigation and recreation purposes often affect lowland lakes situated in or near
densely populated areas. Morphological alterations such as dams and weirs affect mostly
continuity of rivers situated downstream from the lake. On the other hand, ood protection
constructions and drainage of ood plains have created embankments, which can signicantly
change the morphology of lowland lakes. Generally, large scale morphological alterations are
more common in smaller lakes that are surrounded by agricultural and urban areas.
Hydromorphological alterations mostly affect the uppermost littoral zone, which is characterized
by the presence of aquatic macrophytes, although changes in retention time can also indirectly
change the trophic status of whole lake and pelagial communities too. This review focuses on the
relationship between macrophytes and hydromorphological pressures, which is the most commonly
known and investigated.
The Water Framework Directive (WFD) refers to the hydromorphological quality elements of lakes
as hydrological regime and morphological conditions. Hydrological regime is dened as the
quantity and dynamics of ow, level, residence time, and the resultant connection to groundwater.
Morphological conditions are dened as lake depth variation, quantity and structure of the
substrate, and both the structure and condition of the lake shore zone. Hydromorphological
quality elements are only used specically to dene high status in lakes, where these elements
should indicate totally, or nearly totally, undisturbed conditions. For good and moderate status
levels, hydromorphological elements must only be consistent with the achievement of the values
specied for the biological quality elements. Divisions between hydrological regime and
morphological conditions are difcult to make, as these are often interdependent. For example,
level (dened as hydrological) and depth variation (dened as morphological) are highly related.
Therefore hydrological and morphological elements are treated as one in this review.
136 |
6.2 Macrophytes
Macrophytes are one of the key indicators of hydromorphological changes in lakes. Because
macrophytes grow in the littoral zone they are sensitive for changes in water level uctuation
regime. A general zonation of macrophytes can be based on life-form distribution; helophytes
grow in the uppermost zone and isoetids, elodeids and charids occupy deeper areas of lakes. Even
small changes in the dynamics of water level uctuation can affect the distribution and the
elevation of zones. Morphological changes of the littoral zone, caused for example by dredging or
embankments, signicantly disturb the development of vegetation.
Annex V of the WFD outlines three macrophyte-related quality elements that need consideration
in assessing the ecological status of lakes. These are (i) taxonomic composition, (ii) average
macrophyte abundance, and (iii) an ecological assessment which is specic to lake type. This third
requirement, for which reference communities (communities found in non impacted conditions)
need to be identied, also allows for the use of different indices and pressure sensitive species in
different lake types.
Taxonomic composition
In general, taxonomic composition of macrophytes is not a sensitive indicator to describe the
changes in hydromorphology of lakes. However, in many studies it has been shown that macrophyte
diversity is lower in lakes with uctuating water level in North Europe (Rrslett, 1991; Hellsten,
2001) and in Canada (Hill et al., 1998). However, the relationship between water level uctuation
and macrophyte diversity is not simple. An extensive literature survey of Scandinavian lakes
showed that general macrophyte richness correlated mainly with draw-down of water level, but a
regulation amplitude of between 1 and 3 meters supported the highest biological diversity
(Rrslett, 1991). A slight increase in disturbance could even create suitable habitats for European
aquatic macrophytes as noted by Murphy et al. (1990). A similar phenomenon was found in lakes
regulated for hydropower in New Zealand, where an increase in the range of monthly water level
uctuation appears to have increased biodiversity (Riis and Hawes, 2002).
Depth variations are usually related to an articial increase or decrease of water level. Water levels
are increased to extend storage capacity of reservoirs or regulated lakes. A sudden increase of
water level will initiate erosion processes, which lower biodiversity (Nilsson, 1981; Hellsten et al.,
1996). It should be noted that taxonomic composition is a poor indicator of water level increase,
because most of the species are still present after water level increase, although abundance may
differ signicantly (Nilsson and Keddy, 1988; Hellsten et al., 1996). Effects of raised water level
also depend on ageing; after inundation shock of Swedish reservoirs species diversity was highest
30-40 years subsequent to the initiation of the regulation (Nilsson et al., 1997). In most cases
diversity is slightly increased after inundation due to stabilization of the shoreline.
In general, lowering of water level will lead to increased diversity, as found in several studies
(Lohammar, 1949; Toivonen and Nybom, 1989; Rrslett, 1991). The main reason for increased
diversity is that a newly exposed littoral zone or increased shallowness allows the sublittoral zone to
cover the entire water body. Extensive lowering, which affects resuspension in the water body by
allowing waves and currents to reach bottom sediments, can drastically change lake ora, as shown
137
in several studies in the Netherlands (Scheffer, 1998). Several shallow lake studies have demonstrated
a sensitive balance between different species groups (Best, 1987; Van den Berg et al., 1998).
Abundance
Several studies indicate that abundance is a much more sensitive indicator for hydrological
change than species composition (Nilsson and Keddy, 1988; Coops and van der Velde, 1999;
Hellsten et al., 1996; Hellsten, 2001). Generally, water level uctuation affects zonation patterns,
which are a function of the relative abundances of different species with different degrees of
adaptation to stress caused by depth and drying (Pearsall, 1920). Therefore, changes in the
amount of water level uctuation are reected by changes in the distribution of species (Toivonen
and Lappalainen, 1980).
In addition to the range of water level uctuation, the dynamics of the uctuation signicantly
affects the abundance of macrophytes. For example, the timing and range of the spring ood
clearly affects the zonation of sedge species in northern areas (Walker and Wehrhahn, 1970;
Sjberg and Danell, 1983; Hellsten, 2001). The observed increase of common reed (Phragmites
australis) abundance in Scandinavia may be related to lowered early spring water level (Rintanen,
1996; Partanen and Hellsten, 2005). Reeds also benet from stabilized water levels and growth
periods (Coops and van der Velde, 1995; 1999). A general decline of reed beds in Mid-Europe
seems, however, to be related to changes in sediment due to eutrophication (Weisner, 1991;
Clevering, 1999).
Lowering of the water level while a lake is ice-covered will have signicant effects, especially on
large sized isoetids such as Isoetes lacustris and Lobelia dortmanna. Areas where their decline has
been reported include northern Scandinavia (Quennerstedt, 1958; Rrslett, 1984; Rintanen,
1996; Hellsten, 2001) and Scotland (Smith et al., 1987; Murphy et al., 1990). Additional to the
effect of freezing, changes in sediment quality will also signicantly affect their distribution
(Murphy, 2002).
Classication schemes
Very recently, as a direct response to the WFD, and because of the prior lack of suitable classication
schemes, a survey methodology called the Lake Habitat Survey (LHS) was developed in the UK
that directly assesses the hydromorphological elements specied in the WFD. The method is based
on the EMAP guideline and its eld survey method (FOML) developed in the USA. In the LHS
scheme, information on physical habitat (including substrate and riparian vegetation type, but
not species composition) is recorded at sampling plots around the shore, and pressures such as
angling, erosion and grazing are recorded over the entire lake. Data on hydrological regime are
also obtained whenever possible. Apart from the nal report (Rowan et al., 2004), there are no
published reviews of this methodology, however this scheme has the support of the UK authorities
responsible for implementing the WFD and it is intended that it will be adopted throughout the
UK (J. Rowan, pers. comm.). It may also prove to be of use across the rest of Europe, although the
relationship between the LHS score and biological status of lake is not very clear.
138 |
Apart from this new development, there are few classication schemes related to relationships
between hydro-morphological factors and macrophytes. The direct response of Isoetes lacustris to
ice penetration enables its distribution to be used for classication purposes (Rrslett, 1989;
Rrslett and Johansen, 1996; Hellsten, 2001). The deepest growing areas of I. lacustris are also
sharply limited by lack of light and therefore their growing niche is easy to predict (Rrslett,
1988). The distribution of other large isoetids such as Isoetes echinospora, Lobelia dortmanna and
Littorella uniora can also be used for classication purposes, because they are all responsive to
ice erosion and changes in sediment structure (Rrslett, 1989; Murphy, 2002).
A classication based on strategy analysis and the division of species into stress-tolerating, ruderal
and competitive categories has been effective in classifying regulated lakes in Norway (Rrslett,
1989) and in other areas (Murphy et al., 1990). Ruderal species, with high resistance to disturbance,
were typical in shallow water communities of regulated lakes, whereas stress-tolerating species
prevailed in deeper areas.
The effects of depth changes have been generally estimated using simple calculation procedures
to describe the available growth area for macrophytes. Known relationships between the deepest
growth limits of bottom-rooted helophytes have produced a large number of different applications
for Finnish lakes (Hellsten, 2001). Hudon (1997) developed similar relationships between average
water level scenarios and areas dominated by different vegetation types in oodplain lakes of the
St Lawrence River. The vegetated area of the littoral zone has also been used as an index to
describe the trophic status of lakes (Leka et al., 2003).
Models
The relationship between hydromorphological factors and species is usually modelled through
case-dependent correlation models. For example, the effects of water level uctuation depend
essentially on the use of the lake and climate conditions. Rrslett (1989) showed in his review an
analysis of 17 Norwegian regulated lakes in which the species richness (S) followed the equation:
S = 16.4 1.34 W 0.013 H + 0.085 A,
where W = mean annual range of water level (m), H = lake altitude (m a.s.l.) and A = lake area
(km2).
Further in his analysis of 641 lakes from Norway, Sweden, Denmark and Finland, he found that
lake area was the best predictor of species diversity (Rrslett, 1991). A stepwise prediction model
also included hydromorphology related variables such as water level range and lake lowering with
water conductivity and lake elevation values. A predictive model based on discriminant analysis
and vegetation types with environmental background information was developed by Hellsten
(2001). Variables in the stepwise selection were water level duration of summer, duration of
frozen and non-frozen ice pressure zone, bottom substrate and relative erosion rate. The model
produced good results in regulated Lake Ontojrvi, where eight types out of twelve were classied
correctly. In non-regulated Lake Lentua the results were even better, where ten out of fourteen
vegetation types were classied correctly. In this model, variables were more complicated and
more clearly linked to increasing depth.
139
Heegaard et al. (2001) also found relatively promising results by using generalised additive model
(GAM) techniques in lakes in Northern Ireland. Although the models were used in evaluating the
effects of water chemistry on aquatic macrophytes, these predictive models could also be used in
lakes where the water level is uctuating.
6.3 Summary
The littoral zone is a highly varying environment and therefore the relationships between
hydromorphological factors and aquatic macrophytes are often site-specic. However, the
relationship between lowering of ice levels and the destruction of large isoetids is relatively clear
and easy to predict in regulated hydroelectric lakes. Water level uctuation range during the summer
denes the extension of the helophyte zone which can be used as a major determinant of change.
Some of the WFD variables, such as species richness, depend on both water quality and sediment
properties, therefore in nutrient-rich waters it is very difcult to nd relationships between
macrophytes and hydromorphological factors. Nutrient enrichment can also compensate for
degradation caused by uctuating water level. In general, the relationship between
hydromorphological change and aquatic macrophytes is clearer in oligotrophic than eutrophic
lowland lakes.
6.4 References
Best, E.P.H. 1987. The submerged macrophytes in lake Maarsseveen 1: Changes in species composition and
biomass over a six year period. Hydrobiological Bulletin 21:55-60
Clevering, O. 1999. The effects of litter on growth and plasticity of Phragmites australis clones originating
from infertile, fertile or eutrophicated habitats. Aquatic botany 64:35-50
Coops, H., and G. van der Velde. 1995. Seed dispersal, germination, and seedling growth of six helophyte
species in relation to water-level zonation. Freshwater Biology 34:13-20
Coops, H.G.N., and G. van der Velde. 1999. Helophyte zonation in two regulated estuarine areas in the
Netherlands: vegetation analysis and relationships with hydrodynamic factors. Estuaries 22:657-668
Heegaard, E., H. Birks, C. Gibson, S. Smith, and S. Wolfe-Murphy. 2001. Species-environmental relationships
of aquatic macrophytes in Northern Ireland. Aquatic Botany 175-223
Hellsten, S., Marttunen, M., Palomki, R., Riihimki, J., and E. Alasaarela. 1996. Towards an ecologically-based
regulation practice in Finnish hydroelectric lakes - Regulated Rivers: Research & Management 12:535-545
Hellsten, S. 2001. Effects of lake water level regulation on aquatic macrophyte stands in northern Finland
and options to predict these impacts under varying conditions. Acta Botanica Fennica 171:1-47
Hill, N.M., P.A. Keddy, and I.C. Wisheu. 1998. A Hydrological Model for Predicting the Effects of Dams on the
Shoreline Vegetation of Lakes and Reservoirs. Environmental Management 22:723-736
Hudon, C. 1997. Impact of water level uctuations on St. Lawrence River aquatic vegetation. Canadian
Journal of Fisheries and Aquatic Sciences 54:2853-2865
Leka, J., K. Valta-Hulkkonen, A. Kanninen, S. Partanen, S. Hellsten, A. Ustinov, R. Ilvonen, and O. Airaksinen.
2003. Use of aquatic macrophytes for assessing and monitoring the ecological status of lakes Evaluation
of eld survey and aerial photography methods used in the Life Vuoksi Project. Regional Environmental
Publications - Alueelliset ympristjulkaisut (In Finnish) 312
Lohammar, G. 1949. Uber die Vrenderungen der Naturverhltnisse gesenkter Seen. Verhandlungen der
Internationalen Vereinigung fr Theoretische und Angewandte Limnologie 10:266-274
140
Murphy, K.J., B. Rorslett, and I. Springuel. 1990. Strategy analysis of submerged lake macrophyte communities:
an International example. Aquatic Botany 36:303-323
Murphy, K.J. 2002. Plant communities and plant diversity in softwater lakes of northern Europe. Aquatic
Botany 73:287-324
Nilsson, C. 1981. Dynamics of the shore vegetation of a North Swedish hydro-electric reservoir during a 5-year
period. Acta Phytogeographica Suecica 69
Nilsson, C., and P.A. Keddy. 1988. Predictibility of change in shoreline vegetation in a hydroelectric reservoir,
northern Sweden. Canadian Journal of Fisheries and Aquatic Sciences 45:1896-1904
Nilsson, C., R. Jansson, and U. Zinko. 1997. Long-Term responses of river-margin vegetation to water-level
regulation. Science 798-800
Partanen, S., and S. Hellsten. 2005. Changes of emergent aquatic macrophyte cover in seven large boreal
lakes in Finland with special reference to water level regulation. Fennia 183:57-79
Pearsall, W.H. 1920. The aquatic vegetation of the English lakes. Journal of Ecology 8:164-201
Quennerstedt, N. 1958. Effect of water level uctuation on lake vegetation. (Verhandlungen der
Internationalen Vereinigung fr Theoretische und Angewandte Limnologie 13:901-906
Riis, T., and I. Hawes. 2002. Relationships between water level uctuations and vegetation diversity in
shallow water of New Zealand lakes. Aquatic Botany 74:133-148
Rintanen, T. 1996. Changes in the ora and vegetation of 113 Finnish lakes during 40 years. Annales
Botanici Fennici 33:101-122
Rrslett, B. 1984. Environmental factors and aquatic macrophyte response in regulated lakes - a statistical
approach. Aquatic botany 19:199-220
Rrslett, B. 1988. Niche extension of aquatic macrophytes in hydrolakes: Predictive assessments of
environmental impacts. Internationale Revue der Gesamten Hydrobiologie 73:129-143
Rrslett, B. 1989. An integrated approach to hydropower impact assesment. II. Submerged macrophytes in
some Norwegian hydro-electric lakes. Hydrobiologia 175:65-82
Rrslett, B. 1991. Principal determinants of aquatic macrophyte richness in northern European lakes. Aquatic
Botany 39:173-193
Rrslett, B., and S.W. Johansen. 1996. Remedial measures connected with aquatic macrophytes in Norwegian
regulated rivers and reservoirs. Regulated rivers: Research and Management 12:509-522
Rowan, J.S., R.W. Duck, J. Carwardine, O.M. Bragg, A.R. Black, and M.E.J. Cutler. 2004. Development of a
technique for Lake Habitat Survey (LHS): Phase I. Final report of SNIFFER (Scotland and Northern Ireland
Forum for Environmental Research) project WFD40. Available at www.sniffer.org.uk
Scheffer, M. 1998. Ecology of Shallow Lakes. Chapman & Hall
Sjberg, K., and K. Danell. 1983. Effects of permanent ooding on Carex-Equisetum wetlands in northern
Sweden. Aquatic Botany 15:275-286
Smith, B.D., P.S. Maitland, and S.M. Pennock. 1987. A comparative study of water level regimes and littoral
benthic communities in Scottish lakes. Biological Conservation 39:291-316
Toivonen, H., and T. Lappalainen. 1980. Ecology and production of aquatic macrophytes in the oligotrophic
lake Suomunjrvi, eastern Finland. Annales Botanici Fennici 17:69-85
Toivonen, H., and C. Nybom. 1989. Aquatic vegetation and its recent succession in the waterfowl wetland
Koijrvi, South Finland. Annales Botanici Fennici 26:1 - 14
Walker, B.H., and C.F. Wehrhahn. 1970. Relationships between derived vegetation gradients and measured
environmental variables in Saskatchewan wetlands. Ecology 52:85-95
Van den Berg, M.S., H. Coops, J. Simons, and A. de Keizer. 1998. Competition between Chara aspera and
Potamogeton pectinatus as a function of temperature and light. Aquatic Botany 60:241-250
Weisner, S. 1991. Within-lake patterns in depth penetration of emergent vegetation. Freshwater Biology
26:133-142
141
7.1 Introduction
With the word hydromorphological pressures we understand all changes caused by human
inuences to either the ow regime (hydrology) or the morphology of the stream that affect the
biota. The most important hydromorphological pressures are:
building of dams or weirs for hydropower, water supply or other purposes
canalization and/or dredging of rivers or streams to improve drainage or for navigation
weed cutting to improve drainage
abstraction of water directly from the stream or from groundwater for water supply or
irrigation, or diversion (e.g. for hydropower or irrigation).
Other inuences that are not described in detail here include urbanisation, afforestation/
deforestation, draining of wetlands (tiling), transport and supply of water from outside the river
basin to increase river discharge at dry periods, and high discharges of water treatment plants in
small river basins.
142
Weed cutting
Weed cutting is undertaken in many small and medium sized streams to increase the discharge
capacity and prevent the surrounding areas from inundation. River vegetation is rarely found
deeper than 1.5-2 metres and weed cutting is thus a phenomenon related to smaller streams.
When weeds are cut, the water level drops and the water velocity increases, which again may
143
increase the sediment transport and temperature. Bank stability may also be reduced. However,
the physical changes and the impacts on the river ecosystem are strongly dependent on the weed
cutting method.
The immediate effect of weed cutting is a direct loss of plants, which serve as a habitat for
invertebrates and a refuge for sh. The lower water level also reduces the available space and the
habitat diversity. Long-term use of weed cutting changes the composition and structural complexity
of the macrophyte community, which becomes poorer in species and spatially more homogeneous.
Also, substantial changes in composition patterns can develop with an enhanced abundance of
fast-growing species with a high dispersal capacity (Baattrup-Pedersen et al., 2003). A reduced
diversity and structural complexity of macrophyte communities can affect invertebrate and sh
communities negatively. This probably relates to a lower spatial and temporal physical
heterogeneity i.e. less varied substrate composition and more narrow range of ow velocities with
decreasing structural diversity of the macrophyte community (Garner and Bass, 1996). Therefore
loss of macrophyte species and homogenisation of communities as a result of weed cutting may
have cascading effects on the whole stream biota.
http://fame.boku.ac.at.
144
145
0.6
0.4
0.6
0.4
0.2
0.2
0
0.8
Suitability
Suitability
0.8
Adult
Fry/Juvenile
Adult
Fry/Juvenile
0
0
0.2
0.4
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Velocity (m/s)
0.8
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Figure 7.1 Habitat suitability indices for two developmental stages of brown trout (from Bird et al. 1995).
10.00
8.0
1.00
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LIFE Score
Discharge (m3/s)
146
6.5
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96
98
00
Figure 7.2 Flow and the LIFE score in the Waithe Beck in the UK (data from Extence et al., 1999).
Mean ow rank index. A similarly constructed index (MFR mean ow rank) has been developed
by the Environment Agency of England and Wales to relate ows to macrophyte communities
(Soley et al., 2002).
7.5 Summary
Damming, water abstraction, channelisation, dredging and weed-cutting cause major
hydromorphological pressures on river ecosystems. The ecological consequences of damming are
generally well known: A river reach is changed into a reservoir and the river continuity is broken.
The ecological consequences of water abstraction and of changes in river morphometry
(channelisation, dredging, and weed cutting) are known to some extent. However, this knowledge
is not sufcient to establish operational relationships between the degree of pressure (the extent
of anthropogenic impact) and the impacts on river biota needed for the implementation of the
Water Framework Directive (WFD).
7.6 References
Agences de lEau and Ministre de lEnvironnement. 1998. SEQ-Physique: a System for the Evaluation of the
Physical Quality of Watercourses, pp. 15
Allan J.D. 1995. Stream Ecology: Structure and function of running waters. Chapman Hall, London, pp. 388
Arthington, A.H., J.M. King, J.H. OKeeffe, S.E. Bunn, J.A. Day, B.J. Pusey, B.R. Bluhdorn, and R. Tharme. 1992.
Development of an holistic approach for assessing environmental ow requirements of riverine ecosystems.
In: J.J. Pilgram, and B.P. Hooper (Eds.) Water allocation for the environment. The Centre for Water Policy
Research, University of New England, Armidale, pp. 69-76
Baattrup-Pedersen, A., S.E. Larsen, and T. Riis. 2003. Composition and richness of macrophyte communities
in small Danish streams - inuence of environmental factors and weed cutting. Hydrobiologia 495:171-179
Biggs, B.J.F., R.J. Stevenson, and R.L. Lowe. 1998. A habitat matrix conceptual model for stream periphyton.
Archiv fur Hydrobiologie 143:21-56
Bird, D.J., G.W. Lightfoot, and A.P. Strevens. 1995. Microhabitat use by young salmon and trout in a UK chalk
stream. Proc IFM 25th Annual Study Course, Lancaster, 99-114
147
Bovee, K.D. 1982. A guide to stream habitat analysis using the instream ow incremental methodology.
Instream ow information paper 12, U.S. Fish and Wildlife Service Biological Services Program FWS/OBS82/26, pp. 248
Collier, K.J. 2002. Effects of ow regulation and sediment ushing on instream habitat and benthic
invertebrates in a New Zealand river inuenced by a volcanic eruption. River Research and Applications
18:213-226
Dessaix, J., and J.F. Fruget. 1995. Changes of the macroinvertebrate communities in the dammed and
by-passed sections of the French Upper Rhone after regulation. Regulated Rivers: Research and Management
10:265-279
Dunbar, M.J., A. Ibbotson, I. Gowing, N. McDonnell, M. Acreman, and A. Pinder. 2001. Further validation of
PHABSIM for the habitat requirements of salmonid sh. Environment Agency R&D Report W6-036, Centre
for Ecology and Hydrology, Wallingford, UK, pp. 218
Dunbar, M.J., M.C. Acreman, and S. Kirk. 2004. Environmental ow setting in England and Wales Strategies
for managing abstraction in catchments. CIWEM Journal 18:5-10
Dunbar, M.J., and R.T. Clarke. 2004. Generalised LIFE response curves. Centre for Ecology and Hydrology
(CEH) Report to Environment Agency
Duel, H., G.E.M. van der Lee, W.E. Penning, and M.J. Baptist. 2003. Habitat modelling of rivers and lakes in
the Netherlands: an ecosystem approach. Canadian Water Resources Journal 28:231-248
Extence, C.A., D.M. Balbi, and R.P. Chadd. 1999. River ow indexing using British benthic macroinvertebrates:
a framework for setting hydroecological objectives. Regulated Rivers: Research and Management 15:543574
Fleischhacker, T., and K. Kern. 2002. Ecomorphological Survey of Large Rivers. German Federal Institute of
Hydrology, Postfach 200 253, D-56002 Koblenz, pp. 41
Fruget, J.F. 1991. The impact of river regulation on the lotic macroinvertebrate communities of the lower
Rhone, France. Regulated Rivers: Research and Management 6:241-255
Garner, P., and J.A.B. Bass. 1996. The effects of weed cutting upon the biota of a large regulated river.
Aquatic Conservation: Marine and Freshwater Ecosystems 6:21-29
Giller P.S., and B. Malmqvist. 1999. The Biology of Streams and Rivers. Oxford University Press, pp. 368
Growns, I.O., and J.E. Growns. 2001. Ecological effects of ow regulation on macroinvertebrate and periphytic
diatom assemblages in the Hawkesbury-Nepean River, Australia. Regulated Rivers: Research and Management
17:275-293
Hortle, K.G., and P.S. Lake. 1983. Fish of channelized and unchannelized sections of the Bunyip River, Victoria.
Australian Journal of Marine and Freshwater Research 34:441-450
Jorde, K. 1997. kologisch begrndete, dynamische Mindestwasserregelungen bei Ausleitungskraftwerken
(Ecology-based dynamic minimum water requirement regulations for discharge from power plants, in
German). Mitteilungen des Instituts fr Wasserbau, Heft 90, Universitt Stuttgart, pp. 155
Jowett, I.G. 1989. River hydraulic and habitat simulation, RHYHABSIM computer manual. New Zealand
Fisheries Miscellaneous Report 49, Ministry of Agriculture and Fisheries, Christchurch, New Zealand, pp. 39
Killingtviet, ., and A. Harby. 1994. Multi-purpose planning with the river system simulator a decision
support system for water resources planning and operation. In: Proceedings of the rst international
symposium on habitat hydraulics, Norwegian Institute of Technology, Trondheim
Milhous, R.T., M.A. Updike, and D.M. Schneider. 1989. Physical habitat simulation system reference manual version II. Instream ow information paper 26. United States Fish and Wildlife Service, Fort Collins, Colorado
Muhar, S., M. Kainz, M. Kaufmann, and M. Schwarz. 1996. Ausweisungusstypspezisch erhaltener
Fliessgewsserabschnitte in sterreich - sterreichische Bundesgewsser (In German). BMLF, Wasserwirtscha
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Muhar, S., M. Kainz, and M. Schwarz. 1998. Ausweisungusstypspezisch erhaltener Fliessgewsserabschnitte
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BMUJF, Wasserwirtschaftskataster, Wien, pp. 177
Parasiewicz, P., and M.J. Dunbar. 2001. Physical Habitat Modelling for Fish: A developing approach. Large
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148
Toxic pressures
151
8.1 Introduction
The main sources of toxic substances to water bodies in Europe may be categorised as agriculture,
sewage treatment plants, urban runoff, industry, lake/river sediment and landlls. Typically, each
of the sources contributes to the aquatic concentrations of particular substances that may have
an effect on the water environment because of their toxicity. Annex VIII of the Water Framework
Directive (WFD) contains an indicative list of the main groups of pollutants relevant to the
directive. Annex X of the directive lists priority substances selected amongst those, which present
a signicant risk to or via the aquatic environment. The list is to be reviewed every four years.
From the priority substances, priority hazardous substances are selected, emissions and losses
within 20 years. The COMMPS procedure (combined monitoring-based and modelling-based
priority setting scheme) was used in determining the list of priority substances. Thus, models were
used in the selection procedure. The WFD requires the identication of pressures to which water
bodies are subject, with particular regard to substances in Annex VIII of the directive. Further, the
member states are required to assess the likelihood that surface water bodies will fail to meet
environmental quality standards. The WFD denes environmental quality standards (EQS) as
concentrations of pollutants in water, sediment or biota that should not be exceeded in order to
protect human health and the environment.
The classication of water bodies according to ecological status following Annex V of the WFD
includes consideration of specic pollutants. For these, concentrations close to zero for synthetic
pollutants and concentrations close to the background level for non-synthetic pollutants are
required for the water body to have high ecological status. For good ecological status,
concentrations below the EQS are required.
The European Commission is preparing the daughter directive of the Water Framework Directive
(WFD) on chemical pollution control. The preparatory work is carried out in close co-operation
with the EU member states through the AMPS (Analysis and Monitoring of Priority Substances)
expert working group. The European Commission proposed to member states the environmental
quality standards applicable to priority substances. For specic pollutants not on the priority
substance list, the member states shall set EQS for water, sediment or biota. Where possible, both
acute and chronic toxicity data should be considered as a basis for the decision. The base set of
organisms to be considered are algae and/or macrophytes, daphnia (or representative organisms
for saline waters) and sh. Depending on the amount and type of toxicity data available different
safety factors are used in setting the EQS as outlined in the Technical Guidance Document on risk
assessment (ECB, 2003). Data on persistence and bioaccumulation are to be taken into
consideration if they are available.
152
Air
Aerosols
Vegetation
Soil
Water
Aquatic particles
Sediment
153
Table 8.1 Major uses and selected emissions sources of WFD priority substances (modied from Sternbeck
et al., 2003).
Name
4.35
3.17
3.93
5.22
5.86
3.37
2.82
4.15
2.67
3.50
4.26
4.26
2.84
4.66
4.74
2.40
5.31
5.99
Octylphenol,
4-tert-octylphenol
5.50
Hexachlorobutadiene, HCBD
4.72
Benzene
Trichloromethane (chloroform)
1,2-Dichloroethane
Dichloromethane
Tributyltin, TBT
Lead, Pb
Mercury, Hg
Nickel, Ni
Cadmium, Cd
X
X
X
X
X
X
C10-13-chloroalkanes, SCCA
Di(2-ethylhexyl)-phthalate, DEHP
Identied as
Uses or emission sources
priority hazardous
substance
8.39
1.99
1.52
1.83
1.34
7.35
0.73
0.62
-0.57
-0.07
X
X
X
Incomplete combustion
Incomplete combustion
Incomplete combustion
Industrial chemical
Unknown uses
Biocide; unintended formation
Pesticide
Pesticide
Pesticide
Pesticide
Pesticide
Pesticide
Pesticide
Pesticide
Pesticide
Pesticide
Pesticide
Pesticide
Flame retardant
Industrial chemical; forms through
degradation of NP-ethoxylates
Industrial chemical; forms through
degradation of OP-ethoxylates
Industrial chemical; by-product from
chlorinated solvent production
Lubricant; cutting uid
Plasticiser
Incomplete combustion; component i
petroleum products
Solvent
Solvent
Solvent in medical industry
Antifoulant; preservative; stabiliser in plastics;
Numerous
Numerous
Numerous
Numerous
154 |
have been taken from scientic literature and national reports. Data from Swedish databases
(Swedish EPA) have been accessible but other nations databases have so far been difcult to
access. The concentrations of PS found in the available literature sources divided in water phase,
sediments and biota are presented in Table 8.2.
The data availability on the water phase is scarce and, in general, the 33 PS have rarely been
found above detectable concentrations in the water phase. For metals in water there are more
data showing detectable concentrations than there are for the organic substances. For example,
concentrations in the water phase of polycyclic aromatic hydrocarbons (PAHs), atrazine, diuron,
lindane (gamma-HCH), isoproturon, pentachlorophenol (PCP), simazine, polybrominated diphenyl
ethers (PBDE ## 47, 99, 100), hexachlorobutadiene (HCBD), benzene and tributyltin (TBT), are
not frequently found in the literature. More measurements have been performed on sediments, as
the 33 PS are more commonly detected in sediments than in the water phase. Data on PS in the
biota are available in the reviewed sources. The following substances were reported to occur in
detectable concentrations: PAHs, naphthalene, trichlorobenzene, pentachlorobenzene,
hexachlorobenzene (HCB), HCHs, gamma-HCH, isoproturon, PCP, PBDEs, HCBD, DEHPs, benzene,
trichloroethane, dichloromethane, TBT and all the priority metals.
Most of the reviewed studies include concentrations of only a few of the 33 PS. One exception was
a Swedish sediment study performed in an urban area and its surrounding lakes and coastal area
that included measurements of all the 33 PS (Sternbeck et al., 2003). The following substances
were detected in sediments: 4-nonylphenol, 4-tert-octylphenol, PAH, di(2-ethylhexyl)phthalate, C10-13
chloroalkanes, pentachlorophenol, hexachlorocyclohexanes, chlorfenvinphos, polybrominated
diphenyl ethers, tributyltin, As, Cd, Co, Cr, Cu, Hg, Ni, Mn, Pb, Zn, PCBs, DDTs and chlordanes.
Chlorobenzenes were only detected sporadically. Those not detected in any sediment sample
were: alachlor, atrazine, diuron, isoproturon, chlorpyrifos, triuralin, TBBPA, hexachlorobutadiene,
benzene, 1,2-dichloroethane, dichloromethane and chloroform.
To perform measurements of high quality it is essential to have a good strategy. In the Water
Framework Directive a surveillance procedure is described in Annex V for waters. Measurements
of the PS could be carried out in order to determine the concentrations in water, sediment or
biota. The purpose of the measurement determines the sampling strategy such as number of
sampling sites, duration of sampling, type of aquatic media as well as sampling methods.
Measurements could be carried out in order to:
compare water concentrations in relation to EQS
look at the spatial distribution over Europe, in member countries, or in a region
screening
assess time trends and seasonal variations
identify hot spots
assess if the pollution is generated locally or is a result of long range transport
assess whether the pollutants may pose a risk to the ecological system
collect data for model validation.
155
Table 8.2 Concentrations of the WFD priority substances in the water, sediment and biological matrixes found
in the data sources available (Muir and Eduljee, 1999; Skjelkvle et al., 1999; Palm et al., 2001; Palm et al.,
2002; Uln et al., 2002; Kaj and Palm, 2003; Tesfalidet, 2003; berg, 2003, Sternbeck et al., 2003; Bignert
and Carln, 2004; Fjeld et al., 2004; Kaj and Dusan, 2004; Sternbeck et al., 2004; Swedish EPA, 2004). Data
sources are background for all except for the ones marked point* and urban* identied specically from point
and urban sources (n.d. corresponds to substances analyzed, but with values below the detection limit).
Name
PAHs
Anthracene
Naphthalene
Trichlorobenzene
Pentachlorobenzene
Hexachlorobenzene
Alachlor
Atrazine
Chlorfenvinphos
Diuron
Endosulfan
HCHs
(Lindane, gamma-HCH)
Isoproturon
Chlorpyrifos
PCP urban*
PCP point*
PCP
Simazine
Triuralin
PBDE (## 47, 99, 100)
Nonylphenol
Octylphenol
HCBD point *
HCBD
C10-13-chloroalkanes
DEHP
Benzene
Trichloromethane
1,2-Dichloroethane
Dichloromethane
TBT
Pb
Hg
Ni
Cd
max
0.13
n.d.
n.d.
n.d.
n.d.
n.d.
n.d.
n.d.
n.d.
400
n.d.
n.d.
n.d.
n.d.
n.d.
8500
5
5
n.d.
n.d.
0.010
180000
n.d.
n.d.
0.27
n.d.
n.d.
0.05
950
3300
200
0.1
3
0.1
10
1
4.7
15000
9
47600
1070
0.5
600
70
500
0.090
80
950
3.2
0.3
100
2
2
n.d.
4
n.d.
<9
<1
<6
n.d.
n.d.
n.d.
0.06
n.d.
<1
0.2
2
0.02
<1
<3
0.01
30
n.d.
36000
210
150
6
10
3
<13
<2
236
30000
10000
12.5
140
30
<2
14
644
210
23
<6
2.7
5300
140
9
2
0.01
n.d.
0.003
0.001
n.d.
n.d.
n.d.
n.d.
n.d.
5
3.5
n.d.
n.d.
250
10
79
16
16
41
<50
<50
<50
<10
<50
830
481
<50
0.19
20
n.d.
n.d.
0.l4
<10
n.d.
330
1100
<50
<1
0.12
25
<570
<1
<100
n.d.
3.6
30000
10
n.d.
200
430000
3300
35000
<17000
<28
<2800
<57000
5800
430000
3300
63000
7000
0.06
n.d.
350
<10
<50
n.d.
1100
0.3
2
4
4
7
30
<60
<10
36
<50
4500
<340
260
<50
3400
360
74800
1050
3180
66500
156
1.4
105
1.0
104
0.8
ng/g dw
BDE-47, g/kg dw
1.2
103
0.6
0.4
102
0.2
101
0.0
central Stockholm
Coastal
summa-HCH, ng/g dw
157
14
12
10
4
Lakes
central Stockholm
Coastal
158
ng/g lipidvikt
20
Lakes
Lakes - Perch
15
Bysjn
Hjrtsjn
Stensjn
10
5
ng/g lipidvikt
0
15
Coastal
Harufjrden
Coastal-Perch/eel-pout
10
ng/g lipidvikt
Stensjn
5
Bysjn
0
25
Sea
Holmarna
Vderar na
Kvdfjrden
Holmar na
Vderarna
Sea-berring
20
Kvdfjrden
Fladen
15
Hjrtsjn
Fladen
Utlngan
Harufjrden
10
Utlngan
5
0
BDE47
BDE99
BDE100 BDE153
BDE154
Figure 8.5 Screening of PBDEs in sh (ng g-1 lipid) in Sweden (Sternbeck et al., 2004).
Concentrations in water
3
7PCB
Surface
Bottom
Concentration (ng/l)
0
7
15PAH
6
5
4
3
2
1
0
okt-99
dec-99
feb-00
apr-00
jun-00
aug-00
okt-00
Figure 8.6 PCBs and PAHs concentrations in a contaminated bay in the southern Baltic, time trends and
seasonal variations (Palm et al., 2001).
159
presented in Table 8.3. The EQSs are collected from the preliminary Substance Data Sheet for
each PS (AMPS-group). If the water concentrations of PAHs (as 15PAH) in gure 8.6 are compared
with the proposed EQS values in Table 8.3, it can be seen that the proposed EQS value for PAH
6-ring are exceeded in most cases, meaning that this is probably a contaminated site.
Palm et al. (2001) also provided an example of the variation in sediment concentration with
distance from a point source in comparison to background concentrations in a contaminated bay
in the southern Baltic. Figure 8.7 shows the results for PCBs and PAHs. Stations 1-6 are situated
nearest to the source area. Both PCB and PAHs concentrations generally decrease with distance
from the source (Figure 8.7).
Concentrations in water
7PCB
0-20 cm
20-40 cm
40-60 cm
60-80 cm
2
1
0
25
24PAH
20
15
10
5
0
1
10
11
12
13
14
15
16
Sampling station
Figure 8.7 PCBs and PAHs concentrations at different sediment depth in a contaminated bay in the
southern Baltic against sampling station (Palm et al., 2001).
17
160 |
Table 8.3 Environmental Quality Standards for WFD priority substances for inland water (AMPS group,
European Commission, 2004).
Substance
Anthracene
Naphthalene
Trichlorobenzene
Pentachlorobenzene
Hexachlorobenzene, HCB
Alachlor
Atrazine
Chlorfenvinphos
Diuron
Endosulfan
Hexachlorocyclohexanes, HCHs
(Lindane, gamma-HCH)
Isoproturon
Chlorpyrifos
Pentachlorophenol, PCP
Simazine
Triuralin
Brominated diphenyl ethers, PBDE
Nonylphenol, 4-para-nonylphenol
Octylphenol, 4-tert-octylphenol
Hexachlorobutadiene, HCBD
C10-13-chloroalkanes, SCCA
Di(2-ethylhexyl)-phthalate, DEHP
Benzene
Trichloromethane (chloroform)
1,2-Dichloroethane
Dichloromethane
Tributyltin, TBT
Lead, Pb
Mercury, Hg2
Nickel, Ni
Cadmium, Cd3
0.005
0.042
0.02
0.32
0.03
0.22
0.7
0.03
0.5 10-3
0.33
0.061
0.003
0.41
1.3
1.7
12
10
20
0.0001
0.41
1.7
0.08 (40-<100 mgCaCO3 l-1)
0.15 (100-<200 mgCaCO3 l-1)
0.25 (>200 mgCaCO3 l-1)
dissolved Pb; 2no overall MPA/QS can be given; 3as depends on hardness (mgCaCO3 l-1)
Table 8.4 Summary of observed toxic effects of a priority set of substances on biological organisms
belonging to the major trophic groups and biological quality elements as required by the WFD
(cells highlighted indicate observed toxic effects). Phytop.= phytoplankton; Macroph.= macrophytes,
Phytobts= phytopbenthos and periphyton; Zoobts= benthic invertebrates and zooplankton.
Toxic Substance
Alachlor
Anthracene
Atrazine
Benzene
Brominated diphenylethers
Cd and its compounds
Chloroalkanes, C10-13Chlorfenvinphos
Chlorpyrifos
Dichloroethane, 1,2Dichloromethane
Di-(2-ethylhexyl)-phthalate (DEHP)
Diuron
Endosulfan
Endosulfan, alphaHexachlorobenzene
Hexachlorobutadiene
Hexachlorocyclohexane
Lindane, -hexachlorocyclohexane
Isoproturon
Pb and its compounds
Hg and its compounds
Naphthalene
Nickel and its compounds
Nonylphenols
Nonylphenol, 4Octylphenols
Octylphenol, 4-tertPentachlorobenzene
Pentachlorophenol
Polycyclic aromatic hydrocarbons
Benzo(a)pyrene
Benzo(b)uoroanthene
Benzo(g,h,i)perylene
Benzo(k)uoroanthene
Fluoroanthene
Indeno(1,2,3-cd)pyrene
Simazine
Tributyltin compounds
Tributyltin cation
Trichlorobenzenes (1,2,3-; 1,2,4- and 1,3,5-)
Trichlorobenzene, 1,2,4Trichloromethane, chloroform
Triuralin
Phytop
Macroph.
Phytobts
Zoobts
161
162 |
This information is not complete but also the data is incomplete due to technical impairments
(literature sources may report only parameters in the upper effect scale, whereas levels at the lower
scale would be more relevant). Table 8.4 shows a summary of the detected impacts of a set of
priority substances on groups of biological organisms representing different trophic levels of aquatic
ecosystems. All the 33 PS are classied within the reversed proposal for a list of priority substances
in the context of the Water Framework Directive (COMMPS procedure; COMMPS, 1999).
Table 8.5 Examples of existing models, model time-scales, spatial resolution and main eld of application.
Model name
Description/Field of application
Global models
MPI-MCTM
ChemRange
Globo-POP
Distribution model for the assessment of long-range transport and persistence of chemicals
Multi-compartmental mass balance model for evaluation of fate in the global environment
Regional models
Level I,II,III models
Local models
ChemUK
MUM
CeStoc
QWASI
A water-air-sediment exchange model that can be applied to ande lake-or river system
Riverine catchment model (GIS based)
GREAT-ER
163
fate cannot be assembled from monitoring data alone, but can also be captured in mass balance
models. As a result, environmental fate models are widely used to predict contaminant fate and
behaviour proles and are essential tools in the risk assessment process.
Persistent toxic substances (PTS) are included among the WFD priority substances. It is
very important to know how these substances are distributed, magnied and transported within
the environment to evaluate risks and identify sources to be able to reach good water
status. Modelling activities are useful for evaluation of PTS redistribution between various
environmental compartments, long-term trends of environmental contamination, spatial
distribution of concentrations in different media (atmosphere, soil, seawater, and vegetation) and
trans-boundary transport.
Reference
Max Planck Institute for
Meteorology, Hamburg
300 km x 300 km
decades
zonally divided
steady state
Input requirements
Media
key properties
key properties
steady state
www.trentu.ca/cemc
(van de Meent, 1993)
(Wania et al., 2000b)
(Beyer et al., 2000)
steady state
air/water/soil/sed/sh
air/water/soil/sed/sh
air/water/soil/sediment/veg
properties, emission rates
air/water/soil/sediment/veg
properties, emission rates
air/water/soil/sediment/veg.
properties, time-dependent emission rates air/water/soil/sediment/veg
key properties
air, water, soil, sediment, sh
decades
air/water/soil/sediment/veg
yes
www.rivm.nl
www.rivm.nl
decades
air/water/soil/veg
properties, emissions
air/water/soil /sediment/
urban lm
steady state
steady state No
164 |
The Mackay suite of fugacity based models are good examples of steady state mass balance
models, with the simple models relying on equilibrium partitioning and the more complex
assuming that equilibrium is not achieved between compartments. Such multimedia and foodchain models can be used to predict the aquatic concentrations of selected PS when source
information is available, and with knowledge on effect concentrations this is useful for linking the
chemical and ecological status of a water body (Mackay et al., 1983a; Mackay et al., 1983b;
Mackay et al., 1992; Mackay et al., 1996a; Mackay et al., 1996b; Mackay et al., 1996c; Mackay
and Hickie, 2000; Mackay et al., 2003).
There are also examples of dynamic (time-resolved) fugacity based models. Fugacity models driven
by primary emissions are for example used in the U.K to predict and evaluate the historical fate,
behaviour and distribution of PCBs (Sweetman et al., 2002). The model attempts to re-create the
temporal release trend of PCBs over the last 40 years and to replicate the observed historical
trends in soils and sediments.
It is now increasingly accepted that successful management of chemicals in the environment
requires quantitative information on major sources, environmental concentrations, transport
pathways and routes of exposure in the ecosystem. Also esssential are assessments of risk as
determined by the proximity of concentrations or body residues to those at which effects are
observed (see QSAR models, chapter 9 of this book).
At present, several steady-state and dynamic multi-compartmental PTS transport models are
available, which, describe the PTS fate in the environment. The models used, especially those in
Europe, have been summarised in Table 8.5 taken from the report regionally based assessment of
persistent toxic substances regional report region III Europe (UNEP, 2002).
8.8 Summary
The priority substances may originate from a variety of sources. Some are emitted from different
point sources and some are unintentionally formed via e.g. incomplete combustion. Many of them
are banned in Europe, but may still be present in the environment due to their persistence. Because
of atmospheric long-range transport, unregistered use or re-emission, these banned PS may result
in high levels in the water environment in the future.
The WFD has identied 33 priority substances. These substances were selected on the basis of
their risk to the aquatic environment or to human health via the aquatic environment. The present
knowledge concerning the environmental occurrence of these substances is scattered, and differs
widely between different substances. The European Commission is preparing the daughter
directive of the WFD on chemical pollution control. The preparatory work is carried out in close
co-operation with the EU member states through the AMPS (Analysis and Monitoring of Priority
Substances) expert working group. The European Commission proposed to member states the
environmental quality standards applicable to priority substances. At the time of writing this
report, a proposal for priority substance EQS had been submitted but not accepted.
To perform measurements of high quality it is essential to have a good strategy. In the WFD a
surveillance procedure is described in Annex V for waters. Measurements of the PS could be carried
165
out in order to determine the concentrations in water, sediment or biota. The purpose of the
measurement determines the sampling strategy such as number of sampling sites, duration of
sampling, type of aquatic media as well as sampling methods. Due to high measurement costs, the
information concerning chemical fate cannot be assembled from monitoring data alone, but can
also be captured in mass balance models. Environmental fate models are widely used to predict
contaminant fate and behaviour proles and are essential tools in the risk assessment process.
8.9 References
Abou-Waly, H., M.M. Abou-Setta, H.N. Nigg, and L.L. Mallory. 1991. Growth response of freshwater algae
Anabaena os-aquae and Selenastrum capricornutum to atrazine and hexazinone herbicides. Bullettin of
Environmental Contamination and Toxicology 46:223-229
Beyer, A., D. Mackay, M. Matthies, F. Wania, and E. Webster. 2000. Assessing long-range transport potential
of persistent organic pollutants. Environmental Science and Technology 34:699-703
Beyer, A., and M. Matthies. 2001. Criteria for Atmospheric Long-range transport Potential and Persistense of
Pesticides and Industrial Chemicals R &D Project FKZ 299 65 402 E. Schmidt Verlag, Berlin, Germany
Bignert, A., and I. Carln. 2004. Screening of pestisides in sh. Swedish museum of Natural History
COMMPS. 1999. Reviesed proposal for a list of prioroty substances in the context of the water framework
directive (COMMPS Procedure)
Diamond, M.L., D.A. Priemer, and N.L. Law. 2001. Developing a multimedia model of chemical dynamics in
an urban area. Chemospere 44:1655-1667
ECB, 2003. European Chemical Bureau. Technical Guidance Document on Risk Assessment. EUR 20418 EN/1
European Commission. (2004). EAF(7)-06/01 AMPS draft nal report-of the expert group on analysis and
monitoring of priority substances.
Fjeld, E., M. Schlabach, J.A. Berge, T. Eggen, P. Snilsberg, G. Kllberg, S. Rognerud, E.K. Enge, A. Borgen, and
H. Gundersen. 2004. Screening of selected new organic pollutants-brominated ame retardants, chlorinated
parranes, bisphenol A and triclosan. Report 4809, NIVA, pp. 895
Kaj, L., and A. Palm. 2003. Screening of hexachlorobutediene (HCBD) in the environment. IVL report B1542
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9.1 Introduction
The WFD requires the identication of pressures to which water bodies are subject, in particular in
relation to substances listed in Annex VIII of the directive. Further, the member states are required
to assess the likelihood that surface water bodies will fail to meet environmental quality standards.
The WFD denes environmental quality standards as concentrations of pollutants in water, sediment
or biota that should not be exceeded in order to protect human health and the environment.
Annex VIII contains an indicative list of the main groups of pollutants relevant to the directive.
Annex X of the directive lists priority substances selected amongst those, which present a
signicant risk to or via the aquatic environment. From the priority substances, a list of priority
hazardous substances are selected, which shall be subject to a phase-out of discharges, emissions
and losses within 20 years (EC, 2001). The COMMPS procedure (combined monitoring-based and
modelling-based priority setting scheme) was used in determining the list of priority substances.
Thus, models were used in the selection procedure.
In addition to the specically listed substances, the WFD also requires that account is taken of
other toxic substances that may have ecological impact, including river-basin specic pollutants.
For such less common and less investigated pollutants, experimental data about toxicity or
physico-chemical properties is often scarce. Quantitative Structure Activity Relationships (QSARs)
are a potential means to ll data gaps in such circumstances.
9.2 Scope
Potential use of modeling methods in relation to toxic substances and the WFD includes fugacity
modeling and Quantitative Structure Activity Relationships (QSAR):
QSAR models can provide estimates of acute and/or chronic toxicity of substances to
different trophic levels in cases where experimental data are missing
QSAR models can provide data on partitioning, persistence and bioaccumulation in cases
where experimental data are missing.
Fugacity models can provide a link between pressures and concentrations of specic pollutants in
the environment. Thus, they have potential applicability in assessing the likelihood that surface
water bodies will fail to meet environmental quality standards and can be used to estimate
critical target loads. QSAR models are frequently used to estimate physical parameters needed for
fugacity modeling, i.e. partition coefcients, persistence and other parameters, since experimental
data of this type is often scarce.
It is important to note that although there is a strong focus in the WFD on the priority substances;
this review does not only consider these but also other potentially toxic pollutants. Other
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substances besides the priority substances may cause a deterioration in ecological status. QSARs
are potentially more useful in those cases, since experimental data on properties and effects of
the priority substances are, in general, better known.
The major questions that this review tries to answer are outlined below.
What QSAR models are currently available that have a potential use for implementation
of the WFD? Only models with a reasonable degree of successful validation and testing
are considered.
What are possible developments within the near future for QSAR models with potential
use for implementation of the WFD?
What gaps exist with respect to environmental compartments and different classes
of substances?
QSARs are not considered for inorganic compounds such as metals that are not in metallo-organic
form and small inorganic molecules, such as cyanide. The reason for this is that the amount of
structural information for these substances is very limited. Thus there is very limited possibility to
develop QSARs, which is also reected in the lack of available QSARs for these substances (Comber
et al., 2003). The Environmental Protection Agency of the United States of America (US EPA) uses
toxicity estimates based on water quality standards in such cases. Further, the fate and toxicity of
many metals is well understood and chemical speciation models and biological ligand models
may be used to predict their fate and toxicity in many cases. There is a vast literature on QSAR
model interpretation for understanding the mechanism behind toxic action of different substances.
This is not of primary concern for the WFD and thus not considered in this review.
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It is generally accepted that it is important to account for the mode of action (narcosis, electrophilic,
receptor-mediated etc.) when developing toxicity QSARs (Escher and Hermens, 2002; Dearden,
2002; Schultz et al., 2003; Bradbury et al., 2003) since the descriptors and the model must cover
the properties important for that mode of action. This means that QSARs are often, but not
always (Ren, 2003), suitable only for a group of substances having common structural features
and a common mode of action. But QSARs can also be used to infer a likely mode of action from
the chemical structure (Verhaar et al., 1996; Russom et al., 1997).
Models for substance properties other than toxicity are often not called QSARs, since it is not
activity that is modeled. Frequently used names and abbreviations are QSPR (Quantitative
Structure Property Relationships) and QSBR (Quantitative Structure Biodegradation Relationships).
However, the naming is not consistent. In this report we use the QSAR abbreviation for all models
independent of the end-point modeled.
http://ecvam.jrc.it.
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3. How easily are the models results understood and interpreted? (related to 1 above)
4. Has the model received much peer acceptance and what is the models consistency with
scientic theory?
5. How are the models user manual and tutorial?
6. How is the models technical documentation?
7. How is the models interactivity, user-friendliness and suitability for end-user participation?
8. How is the models exibility for adaptation and improvement?
These principles have been applied in the evaluation and analysis of QSAR models in this report.
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2. Decision for further testing. When the PEC/PNEC ratios derived by QSARs are >1 this is
considered an indication that more testing is needed (PEC: predicted environmental
concentration; PNEC: predicted no effect concentration).
3. Establishing specic parameters. Acceptable QSARs can be used to estimate parameters
needed as input for the PEC calculation.
4. Effects of potential concern. Acceptable QSARs can be used for preliminary assessment
of end-points that are not part of the base set of data.
The US EPA and other US authorities routinely use QSARs in chemical risk assessment (Walker,
2003). The Toxic Substances Control Act (TSCA) requires that the TSCA interagency testing
committee use QSARs to predict toxicity in the absence of data. Further, the US EPA uses QSARs
in combination with expert opinion for risk assessment of new chemicals (Comber et al., 2003).
The OECD Manual for Investigation of HPV (high production volumes) chemicals (OECD, 2003)
states that when no information is available for a given data element, calculation or estimates
derived from Quantitative Structure Activity Relationships (QSARs) can sometimes be provided.
The recommended QSARs for ecotoxicity are those implemented in the ECOSAR software package
but other models can be used as long as an indication of the quality of the methods used is given.
Also, QSAR predictions must be accompanied by experimental data for a close analogue. QSARs can
also be used for vapour pressure, KOW and water solubility if tests are impractical for some reason.
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The uncertainty of reference data is important to consider when developing QSARs. ECETOC (1989)
reports results from inter-laboratory testing indicating coefcients of variation (relative standard
deviations) of 5-80% with a typical value of around 50% for a range of biological toxicity tests.
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predictions are normally within a factor of 2-3 from the experimental value. Daphnia magna
models exist for four classes of compounds and cross-validation indicates an error of 0.5-1.5 log
units. TOPKAT determines whether the submitted structure belongs to the so-called Optimum
Prediction Space (OPS) of the model in order to evaluate the reliability of the QSAR-based
assessment. The independent comparative study by Moore et al. (2003), discussed further below,
indicates that TOPKAT performs very well within its OPS but that this space is rather limited, i.e.
that the models are only valid for a limited set of substances.
Multicase5 has a module for Pimephales promelas LC50 predictions. The model is built from 479
training substances. Klopman et al. (2000) used Multicase to develop a model for the same endpoint based on 685 substances. The model incorporates the concept of a baseline activity as one
of the parameters for the correlation as well as others parameters such as the presence of
biophores, hardness-softness parameters, and other characteristics determined from quantum
mechanical calculations. This model is used by the Danish EPA for prediction of sh toxicity. The
performance was not veried by independent test data to our knowledge.
Kaiser and co-workers have developed probabilistic neural network (PNN) models for large diverse
sets of chemicals for Daphnia Magna (Kaiser and Niculescu, 2001), Tetrahymena pyriformis
(Kaiser et al., 2002) and Pimephales promelas (Kaiser and Niculescu, 1999). They used a large
number of substances and structure fragment based descriptors to build models that are valid for
a variety of toxic modes of action. Model validation shows excellent performance and the large
number of substances in the training set means that the applicability domain of the model is
larger than for many other models. The QSAR for Pimephales promelas (fathead minnow) has
been commercialised by TerraBase Inc6.
Furusj et al. (2003; 2006) have developed models for acute toxicity to green alga 96 h
(Selenastrum capricornutum growth rate inhibition EC50), Daphnia magna (48 h immobilisation
EC50) and sh (Lepomis macrochirus and Leuciscus idus 96 h toxicity LC50). They use an outlier
detection methodology to ensure reliable predictions and thus manage to produce a prediction
standard error of 0.5 log units on test data for substances within the valid chemical space of the
model. For substances outside the prediction space, the error is larger but the model automatically
provides diagnostics that shows if the prediction is accurate or not.
A review by Moore et al. (2003) has evaluated the performance of six QSAR packages for acute
aquatic toxicity: ECOSAR, TOPKAT, a Probabilistic Neural Network (PNN; Kaiser and Niculescu,
1999), a Computational Neural Network (Eldred et al., 1999), ASTER and OASIS7. Some of these
require input in the form of log KOW, which was calculated by the CLOGP8 software discussed
elsewhere in this report. PNN and ECOSAR perform best in this study and are also the only
packages that are able to produce predictions for all 130 test substances. Still the coefcient of
variance is relatively low (r2~0.3). TOPKAT and OASIS have a large advantage compared to other
packages, they produce prediction outlier diagnostics, i.e. indicates if the model is valid for the
http://www.multicase.com.
http://www.terrabase-inc.com.
7
http://omega.btu.bg/.
8
http://www.biobyte.com.
5
6
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substance in question (this is called Optimum Prediction Space, OPS, in TOPKAT). For TOPKAT
there is a huge difference in performance between substances within the OPS (47 out of 127
substances) and those outside the OPS. The performance of TOPKAT for the 47 OPS substances is
far better than for any other package evaluated (r2~0.6). For OASIS, 105 substances do not
generate warnings but the difference in performance between those and the 15 substances with
warnings is much smaller than for TOPKAT, which indicates that the outlier detection in OASIS
does not perform so well. The test set used in the evaluation by Moore et al. (2003) is heavily
weighted with low molecular weight substances that act by non-polar narcosis. A larger and more
diverse test set is needed to evaluate performance for substances with other modes of action.
The results of both evaluation studies discussed above (Moore et al., 2003; OECD, 1994) are
based on the assumptions that the reference toxicity data (LC50 and EC50) are accurate. However,
this is denitely not the case. In both studies sh LC50 data are, for several species, under nonstandardised test conditions. This should not affect the ranking but means that the performance
of the methods is likely to be better than indicated in the studies, since the reported prediction
errors are actually a sum of the model and experimental errors.
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Sediment toxicity
No models covering more than a very limited group of substances that predicts toxicity to
sediment-living organisms have been found. Approaches to convert PNECwater predicted by QSARs
to PNECsediment based on pore water concentrations calculated from equilibrium theory have been
used. An example of this approach in combination with QSARs is the one by van Leeuwen et al.
(1992) at the University of Utrecht. The authors have used QSAR estimates of toxicity of narcotic
chemicals to estimate PNECs from means of extrapolation methods. Equilibrium partitioning
theory was used to derive PNECs for aquatic sediments and internal toxicant concentrations for
aquatic organisms. Calculations were carried out for 102 narcotic compounds. The 1999 revised
proposal for priority substances (Klein et al., 1999) refers to the TGD on risk assessment (ECB,
2003) for calculation of PNECsediment from PNECwater for organic substances. The proposed procedure
is not applicable for metals.
Endocrine disruption
Endocrine disrupting chemicals (EDCs) are an area of growing concern in chemical risk assessment.
Most of the end-points related to endocrine disruption used in QSAR modelling are in vitro tests
related to receptor binding or biological effects of receptor binding, e.g. gene activation. QSARs
are considered important and potentially useful due to the complexity and cost of in vitro and in
vivo tests for endocrine disruption.
The current status of QSARs for endocrine disruption (Schmieder et al., 2003) are that most
models are developed for specic substance groups. Some models have been developed based on
diverse sets of chemicals with the purpose of screening new chemicals for EDCs. Focus is on the
human estrogen receptor (hER) with few applications to other human receptors and ERs from
rodents and calves. No QSARs for endocrine disruption in aquatic organisms have been found.
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http://ecb.jrc.it/existing-chemicals.
http://www.epa.gov/oppt/exposure/docs/episuitedl.htm.
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recommends these models for biodegradation but states that many substances are falsely
predicted to degrade fast, so that only predictions indicating slow biodegradation should be
considered (ECB, 2003).
2. Estimates the time required to achieve primary and ultimate biodegradation on the scale of
hours, days, week, months or longer according to a method described by Boethling et al. (1994).
3. Predictive models for assessing a chemicals biodegradability (readily degradable, not readily
degradable) in the Japanese Ministry of International Trade and Industry (MITI)
biodegradation test (Tunkel et al., 2000). These models were developed using larger data sets
than the above and were validated with external data giving approximately 80% correct
classication.
4. The predictions are combined in a battery approach to obtain a summary prediction of
whether or not the substance is readily biodegradable.
The ECETOC report on available QSARs (ECETOC, 2003) states that BioWin is a simple and very
well working model. It should be noted that BioWin contains six different models that can give
non-uniform results, which hinders easy usage. A recent study shows that although individual
models can misclassify substances the risk of false positives, i.e. to predict a substance as readily
degradable although it is not, can be signicantly reduced by using several models from Biowin
in a battery (Boethling et al., 2004).
The TOPKAT package has an aerobic biodegradability module, consisting of four structurally based
sub-models. A single study which reported the biodegradability of 894 compounds, as assessed by
the MITI test protocol number I, was used to develop these models. The discriminant models
estimate the probability of aerobic biodegradation, where probability values between 0.3 and 0.7
refer to an indeterminate region. TOPKAT uses prediction outlier diagnostics to determine whether
the submitted structure belongs to the Optimum Prediction Space (OPS) of the model, which
indicates a reliable prediction. No external validation has been reported to our knowledge.
Expert systems can be used to predict degradation pathways for organic substances and assess
persistence. Two commercially available expert systems are CATABOL from the Laboratory for
Mathematical Chemistry in Bulgaria and META from Multicase Inc. (see notes 5 and 7). The
CATABOL software uses a mechanistic modelling approach for quantitative assessment of
biodegradability (Jaworska et al., 2002), which predicts biodegradation pathways of chemicals
and classies them as readily degradable or not. CATABOL is unique in that it considers the full
biodegradation pathway and not only the parent compound. META can be used to predict
biodegradation pathways for both anaerobic and aerobic environments. The methodology is an
expert system based on fragment data and transformation rules (Klopman et al., 1995).
OECD (OECD, 1993b) published an early biodegradability QSAR report in 1993. The authors
concluded that only a few of the 75 models evaluated (most of them class specic) can be
recommended for predictive purposes. In most cases the poor performance is due to bad training
data: inhomogeneous end-point determinations or restricted data sets.
ECETOC (ECETOC, 2003) has compiled validation data for BioWin (MITI end-point), META and
CATABOL. The results showed similar performance for the three programs with approximately
80% correct classications into readily or not readily degradable.
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A different and potentially more accurate approach is to use a multimedia/fugacity type model
to estimate the total half-life of the substance in the system studied. Different approaches are
possible as discussed by Mackay et al. (2003) but the advantage is that explicit consideration is
given to the partitioning of the substance in the environment. The multimedia model would then
need QSAR estimates of partitioning coefcients as well as half-lives or degradation constants in
different media including biodegradation.
Photolysis. Photolysis in water can be a signicant degradation pathway, especially for substances
that are not biodegradable. The EU TGD currently does not recommend any QSAR models for this
end-point, since the existing models do not meet the requirements (ECB, 2003). Mill (2000)
further discusses QSAR development for aqueous photolytic reactions.
Hydrolysis. The EU TGD (ECB, 2003) recommends ve separate class specic QSARs for
brominated alkanes, esters, carbamates and benzonitriles, which are based on electronic and
steric constants. No validation of the models has been found in the literature. OECD (OECD,
1993a) recommends some class-specic methods based on Hammet and Taft constants but note
that the models do not cover more than a very small amount of chemicals. HydroWin, which is a
part of the EpiSuite program (see footnote 10), is applicable for certain chemical classes. The
program estimates base and acid catalysed hydrolysis rate constants. No validation of the models
has been found in the literature.
Chemical oxidation and reduction. Canonica and Tratnyek (2003) have reviewed QSARs for
oxidation rate constants in aquatic environments. They conclude that many of the reactions
treated in the literature are not relevant for oxidation in the natural environment. Environmentally
relevant oxidants include excited triplet states of dissolved organic substances and photogenerated singlet oxygen. For the latter, a number of Hammet constant based QSARs exist for
individual groups of chemicals.
QSARs for reduction reactions relevant for the aquatic environment describe dechlorination and
nitro group reduction (Tratnyek et al., 2003). A problem with models yielding observed rate
constants is that the systems for which the experiment is carried out are usually not very well
dened, which makes it difcult to use these QSARs in practice. Models of well-dened systems
also exist, but unfortunately these are not straightforward to use in practice since they are usually
unrepresentative of the complexity of systems occurring in the environment. Thus, the underlying
problem, which is not a QSAR issue, is that the chemical agents responsible for reduction and
oxidation in the environment vary in concentration and type and are often difcult to quantify.
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log KOW as the sole descriptor but it has been noted that the correlation between BCF and log KOW
breaks down at log KOW values over 6-7 (OECD, 1993a).
The EU TGD on risk assessment (ECB, 2003) recommends a method implemented in the EUSES
software (footnote 9). A linear QSAR for calculation of BCF in sh from KOW was derived for log
KOW<6 and is only valid within this range. Validation with a 267-substance test set gave a standard
prediction error of 0.58 log units. A non-linear QSAR is used for log KOW>6 but the accuracy is lower
than for the linear model. The models are not applicable for ionic substances and organometallics.
ECETOC (ECETOC, 2003) raises a number of questions relating to these models and the data they
are based on and recommends careful assessment of the model and the purpose of its use.
BCFWIN is a part of the EpiSuite software and is publicly available (see footnote 10). The BCFWIN
method published by Meylan et al. (1999) classies a compound as either ionic or non-ionic. The
QSARs for non-ionic compounds use log KOW and structural correction factors to predict BCF. The
correction factors allow for correction of substance metabolism to some extent (ECETOC, 2003), which
is advantageous. Different QSARs are used depending on the KOW range. It is noted that organometallics,
substances with long chain alkyls and aromatic azo compounds require special treatment.
CEFIC, the European Chemical Industry Council, validated the BCFWIN model using a test set of
50 substances (ECETOC, 2003). The results show reasonable predictive ability of BCF and about
70-80% correct classication of bioaccumulation potential. It should be noted that several of the
substances included are expected to be bio-transformed and consequently predictions based on
log KOW are expected to be conservative. The RMSEP for BCF was 0.96 log units. The authors note
that the BCFWIN model can be expected to give both false positives and false negatives in
classication but still recommend it over the other models evaluated.
Mackay et al. (2003) indicate that although BCFWIN is a successful model, mechanistic models
are preferable. This is especially true for substances that are metabolised readily. QSARs are likely
to overestimate bioaccumulation for these. It should be noted that the mechanistic models are
heavily dependent on QSAR derived partitioning data, as discussed in section 9.3. The POPs
software (Laboratory of Mathematical Chemistry, Bourgas University, Bulgaria) implements a
method for evaluation of sh bioaccumulation potential by a non-linear BCF model. The model is
dened within a large range of hydrophobicity (Dimitrov et al., 2002).
12
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has a reported uncertainty of 0.3 log units (ECETOC, 1989) and all reported QSAR prediction
uncertainties below must be compared with this value. The approach used in KowWin (Meylan
and Howard, 1995) is based on atom/fragment contributions and has been reported to give an
RMSEP of 0.31 log units for 6055 test substances. An independent study by Eros et al. (2002)
indicates that the RMSEP is at least twice that gure for new data.
A recent comparison between some available software packages and a new method (Eros et al.,
2002) revealed that the classic and freely available software package CLOGP v3 performs well
in most cases. It uses fragment contributions and correction factors to account for fragment
interactions and builds on a database of thousands of compounds. The model is thus applicable
for substances in a large chemical domain. The study indicated a prediction standard deviation of
about 0.6 log units (a factor 4) for substances unknown to the model. This model is also the one
recommended by the OECD in a study in 1993 (OECD, 1993a). Both CLOGP and KOWWIN are
recommended by the EU in the TGD for risk assessment (ECB, 2003).
ECETOC (ECETOC, 2003) refers to a validation study using independent test data where the
prediction errors for SPARC, KowWin and CLOGP were 0.33, 0.34 and 0.29 log units respectively.
In another study (ECB, 2003), the prediction standard deviation is approximately 0.3 log units for
both CLOGP and KowWin for a 1166 substance test set. The accuracy is higher for KowWin for log
KOW>5, while CLOGP gives better estimates for log KOW<0. It should be noted that the CLOGP
program v3 cannot process structures that contain tertiary amines, thiophosphates, phosphites,
phosphines and some other fragments because they are missing in the fragment database.
Also, salts and substances with formal charges are not handled (ECB, 2003).
Methods based on molecular descriptors, as opposed to atom or fragment-based contribution, at
least partly overcome problems that appear when new fragments, for which no contribution is
available, are introduced (Katritzky et al., 2000). Methods based on solvatochromic descriptors
have good performance but these descriptors have to be determined experimentally, which makes
the practical use of the models very limited.
A good and applicable QSAR model based on molecular descriptors (electrotopological state
indices; Gombar and Enslein, 1996) is implemented in the TOPKAT software. A large advantage
is the prediction diagnostics, called optimum prediction space (OPS). The authors report a
prediction error of 0.27 and 1.35 log units for substances inside and outside the OPS respectively,
which clearly indicates the benets of prediction diagnostics.
ALOGPS (footnote 14) is freely available over the internet and uses atom counts and
electrotopological state indices and an articial neural network model to estimate log KOW for
substances based on their structure (Tetko and Tanchuk, 2002). Validation with an independent
test indicates an RMSEP of approximately 0.5 log units. An interesting option is to include a
library of molecules with known KOW that are similar to the ones one wants to predict. This improves
the performance substantially but it is of course not certain that such data is available.
Soil sorption - KOC. Soil sorption is a fundamental process that has a large impact on the
availability, fate and persistency of substances in the environment. Sorption coefcients
quantitatively describe the distribution of a chemical between an environmental solid and the
aqueous phase that it is in contact with. Sorption can take place by a number of mechanisms and
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sorption coefcients depend on a large number of factors such as organic matter quantity and
type, clay mineral content and type, particle size distribution, pH, temperature and dissolved
organic material. Fortunately some generalisations can often be made that facilitate the
calculation and measurement of sorption coefcients. Sorption coefcients are normally assumed
to represent equilibrium but sorption kinetics can play an important role for some slowly absorbing
substances, especially in fast processes such as soil resuspension. Incorporation of kinetic
considerations is an important area for future work (Doucette, 2003). Linear sorption behaviour
is usually assumed, although non-linear sorption can be accounted for using the Freundlich or BET
type models.
For organic substances, which are the topic of this review, and especially neutral and hydrophobic
substances, sorption is highly correlated or directly proportional to organic matter content of the
solid. As a consequence, organic carbon normalised sorption coefcients, KOC, are used.
This approach works reasonably well for a large number of organic chemicals and is the most
popular for use in environmental applications. For ionizable substances and for soil/sediment
with a low organic content (<0.1%) other approaches should be used (Doucette, 2003).
When evaluating the performance of QSARs for KOC, consideration must be given to the accuracy
of experimental KOC determinations for two reasons. The rst is that the QSAR model is an
alternative to more expensive and time consuming experimental determinations and hence their
relative performance is of interest. The second reason is that the prediction errors estimated from
model validation are inuenced by inaccurate reference values since it is the difference between
these and the predictions that are used to estimate the error. Usually unstandardised methods for
experimental determination of KOC are used, but even for the ASTM standardised method a
coefcient of variation of around 50% can be expected (Doucette, 2003), which corresponds to
0.2-0.3 log units.
The most widely used QSARs for KOC are based on simple correlations with KOW or water solubility
(SW). Some also require the melting point as an input. General or class specic models are available
for examples see the review by Doucette (2003). Class specic models often have a better
performance if they are available for the substance in question. Generally, the accuracy of models
for log KOC is within 0.3-1 log units if accurate values of KOW or SW are available (Doucette, 2003).
If experimental KOW and/or SW are not available, calculated values can be used but this lowers the
accuracy of the KOC predictions.
The system of class-specic QSARs for calculation of KOC from KOW developed by Sabljic et al.
(1995) are recommended for KOC prediction in the EU TGD on risk assessment (ECB, 2003). The
EUSES software (footnote 9), contains an implementation of these that can be used in the absence
of experimental soil sorption data. Calibration errors for different models range from 0.2-0.5 log
units. To our knowledge, the methods have not been validated with external data.
Methods that are based on molecular structure and do not use KOW or SW as descriptors do not
suffer from lack of experimental data for these parameters. Methods based on molecular
connectivity indices (MCI) are popular but their domain is often limited to a specic group of
substances, which makes them less generic. Meylan et al. (1992) have used MCIs in combination
with fragment based polar correction factors to overcome this drawback. Their model is
implemented in the PCKOCWIN model of the EPI Suite software (footnote 10).
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In addition, methods based only on fragment contributions can be used. Tao (1999) developed
such a model with a reported average test set prediction error of 0.47 log units, which is considered
acceptable compared to other approaches and accuracy of experimental reference values. Other
methods for estimating KOC based on the quantum mechanical descriptors, molecular surface
area, characteristic root indices (CRI), linear solvation energy relationships (LSER) and
chromatographic retention times are considered less useful with respect to either performance
requirements or from a practical viewpoint and are not discussed further.
Air-water partitioning. Dearden and Schuurmann (2003) summarised some studies that all point
out the great deciency of experimentally determined Henrys law constants (HLCs) for
environmentally relevant substances, which means that QSAR models are of great relevance. Two
recent reviews cover methods and models for calculating HLCs (Staudinger and Roberts, 1996;
Dearden and Schuurmann, 2003). HLCs can theoretically be approximated by the ratio of vapour
pressure and aqueous solubility but the use of experimental values in this relation can hardly be
considered predictive (Dearden and Schuurmann, 2003), due to uncertainties in the experimental
values and non-ideal behaviour of the substance. Methods for measuring non-ideality (activity
coefcients) experimentally exist but also suffer from poor accuracy for many environmentally
relevant substances (Staudinger and Roberts, 1996). Approaches that do not use experimental
data as descriptors are interesting from a practical point of view, since good quality experimental
values of physical properties are often unavailable.
HenryWin is a part of the EpiSuite software (footnote 10) that can estimate HLCs. Two methods
are used, based on bond (Meylan and Howard, 1991) and group contributions respectively.
Validation of the bond method with a test set of 1650 substances gave an RMSEP of 1.43 log
units but a lower RMSEP of 0.79 log units was reported for substances with higher volatility than
what is considered non-volatile from water, which is much more relevant for the practical use of
the model. The group method does not usually perform as well as the bond method. An independent
comparative study of several methods and models for a data set of 700 substances (Dearden and
Schuurmann, 2003) indicated that HenryWin was the best performing of the 12 tested methods
with a standard error of 1.03 log units. Also Staudinger and Roberts (1996) recommend the two
methods implemented in HenryWin among available general (diverse) QSARs. Poor performance
for large molecules is noted in the EU TGD (ECB, 2003) but HenryWin is still the recommended
QSAR model for air-water partitioning in the TGD.
Water solubility. Water solubility SW is relevant for the partitioning of substances in the
environment and required as input to most fate models. Temperature effects on SW are usually not
accounted for by QSAR models available today, which is a limitation in their applicability and an
area for further research. There are three major groups of models for prediction of SW: (1) based
on measured physicochemical properties (most importantly KOW, MP, BP and molar volume), (2)
based on group contributions and (3) based on descriptors calculated from molecular structure.
WsKowWin is a part of the EpiSuite software that can estimate water solubility based on log KOW,
molecular weight and (if available) melting point (Meylan et al., 1996). Validation with 817 test
substances gave an RMSEP of 0.62 log units and an absolute mean error of 0.48 log units.
WaterNT was recently added to the EpiSuite software. It uses a fragment contribution method
and correction factors to estimate water solubility. The standard deviation of the predictions for
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training data is 0.34 log units but external validation with nearly 4000 substances gave an
RMSEP of 0.87 log units.
The freely available SPARC model (footnote 13) uses linear free energy relationships to predict SW.
A recent but limited comparison (Letinski et al., 2002) indicates that SPARC performs better than
WsKowWin. Also ALOGPS (footnote 14) is freely available over the internet and uses
electrotopological state indices and an articial neural network model to estimate SW for
substances based on their 2D structure16 (Tetko et al., 2001). Validation with an independent test
set gave RMSEP of 0.63 log units.
QikProp (Jorgensen and Duffy, 2002) is designed for drug discovery purposes and can predict SW
with RMSEP of 0.70 log units. QikProp requires structure optimisation (e.g. by molecular mechanics)
to give accurate results. The OECD report from 1993 recommends a method by Isnard and Lambert
(1989) with RMSEC=0.58 but with no external validation. Numerous other methods for prediction
of SW exist of which some are summarised in Katritzky et al. (2000). Most of them are not validated
well enough to assess their performance for structurally diverse sets of new substances.
Melting point. Melting points are normally not of interest by themselves in determining the
environmental fate of chemical substances but are used as an input in many fate models due to
their relation to solubilities, boiling point and vapour pressure. Melting point can be expected to
be a difcult property to model due to the complex interactions present in the solid state. On the
other hand, they are usually quite easy to measure accurately experimentally, so the interest for
QSARs with this end-point is probably smaller than for other properties. However, there is a need
for MP models since many environmentally interesting compounds lack experimental MPs
(Dearden, 2003).
Most published QSARs for melting points are only valid for a limited set of substances (Katritzky et al.,
1997; Katritzky et al., 2000; Dearden, 2003). Models for more diverse sets are of greater interest in
the current context but, as noted below for MpBpWin, model performance is often disappointing, e.g.
with RMSECs of 30 K for a model covering mono and disubstituted benzenes (Katritzky et al., 1997).
Dearden (2003) reviewed recent QSAR models and SW packages for MP prediction. The three SW
packages tested (MpBpVp, ChemOfce, Propred) had very similar performances with RMSEP between
25 and 27 K for 100 small organic test substances. MpBpWin is a part of the EpiSuite software and
can estimate melting points with two different methods: the Joback method (Joback, 1984) and the
Gold and Ogle method, which is a simple relation between melting point and boiling point. The
program uses a weighted average on these two with weights depending on the type of structure.
The accuracy of the MpBpWin estimate was tested on a 666 compound data set containing a
diverse mix of compounds. The results were Q2=0.73 and RMSEC=59 K. The accuracy was further
tested on a data set of 1379 different compounds including many complex pharmaceutical
chemicals and pesticides. MpBpWin estimates yield Q2=0.71 and RMSEP=58 K, which is very
similar to the results for the 666 compound data set. Thus, MpBpWin estimates of melting point
are at best useful for screening; a prediction standard deviation of 60 K cannot be considered a
quantitative estimate.
16
184
QSAR estimated melting points can only be recommended for screening purposes (at best), which
is also noted by the OECD (OECD, 1993a).
Boiling point. MpBpVp calculates boiling points using an adapted Stein and Brown method
(Stein and Brown, 1994) based on group contributions with a correction term. The Stein and
Brown method was derived from a training set of 4426 diverse organic compounds with a standard
deviation of 24.6 K. It was then validated on an external test data set of 6584 compounds with
the following statistical accuracy: average absolute error = 20.4 K; standard deviation = 38.1 K;
average error = 4.3%. The extensive and diverse validation set makes these performance estimates
reliable for predictions of new compounds.
Dearden (2003) reviewed and tested 6 software packages that can be used for BP prediction and
are available commercially or free of charge. The test was done using 100 small organic substances.
MpBpVp was one of the packages tested and the resulting average absolute prediction error was
13.8 K, which is lower than the number obtained from the larger and more diverse data set. SPARC
produced an average prediction error of 6.3 K for the same (limited) data set, which indicates
superior performance. No study showing the applicability for more diverse sets have been found.
A number of models for boiling point estimates have been developed by Jurs and co-workers
(Egolf et al., 1994; Wessel and Jurs, 1995). The models have, in general, good performance in
their applicability domain with RMSEC values around 12 K for rather large diverse data sets. The
good performance originates partly from the use of so-called charged partial surface area (CSPA)
descriptors, which are 3D descriptors that require specic software for calculation. The models are
thus not straightforwardly applied today. Several other models based on linear QSAR are reviewed
in Katritzky et al. (2000) and Dearden (2003) but the validation of these models is not satisfactory
or not described in enough detail to estimate their reliability.
Non-linear models, primary neural network based models, have received increasing attention.
These types of models seem promising and have lower RMSECs (Katritzky et al., 2000; Dearden,
2003) but as with the linear models the validation is not sufcient. Further validation studies of
existing models to determine their precision and domain of applicability are needed.
Vapour pressure. Vapour pressure (VP) is required as an input to fugacity calculations and can be
used (together with SW) to estimate HLC. VP is difcult to determine accurately experimentally for
low boiling compounds. Katritzky et al. (2000) report some different QSAR models for VP. The
models based on diverse sets of chemicals (Liang and Gallagher, 1998; Katritzky et al., 1998) are
most relevant and have prediction errors of 0.3-0.5 log units. The models use quantum chemical
descriptors which means that quantum mechanical modelling software is needed to use them.
The models are not readily available as software packages.
QSAR methods and software packages for VP estimation were also recently summarised by
Dearden (2003). Most models discussed are valid for diverse substances and show relatively high
accuracy (estimated errors around 0.4 log units, which is considered good given the large span in
VPs involved). Four software packages, available commercially or free of charge, were tested using
100 small organic substances. One of the reviewed software packages is MpBpVp. MpBpVp can
estimate vapour pressures using different methods: Antoine (Lyman et al., 1990) and modied
Grain (Lyman, 1985). For solids, the modied Grain estimate is the suggested VP. For liquids and
185
gases, the suggested VP is the average of the Antoine and the modied Grain estimates. Boiling
and melting points are needed and QSAR estimates of these are used if experimental values are
not available. MpBpVp showed an average absolute prediction error of 0.285 log units while
SPARC produced an average prediction error of 0.105 log units.
In the original work, the MpBpVp VP predictions were validated on an 805 compound data set.
In the validation, all the boiling and melting points used for the VP estimates were estimated by
MpBpWin to introduce the maximum amount of error that would be encountered during normal
use. The validation gave Q2 = 0.94 and RMSEP = 0.72 log units, which is higher than the errors
reported by Dearden (2003) for the more limited data set. It is likely that much of the error is
introduced by the known poor estimates of boiling and melting points. The same problem, as
discussed for SW and HLC, is that only models giving predictions valid at 25C are available,
applies to most VP QSAR models (Dearden, 2003).
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Toxicity
Effect and no-effect concentrations. The availability of QSARs for chronic predicted no-effect
concentrations (NOEC) is very limited. In the absence of measured NOECs, PNECs are frequently
calculated by using an assessment factor and predicted acute effect concentrations. In risk
187
assessment within the EU, an assessment factor of 1000 is used to reect the large uncertainty in
extrapolating acute effect data to no-effect concentrations. If chronic test data are available,
lower assessment factors can be used (ECB, 2003).
The safety margin inherent in the assessment factors is adequate for risk assessment where conservative
estimates are needed. If likely rather than conservative estimates of PNEC are needed as will be the
case for at least some applications related to the WFD this procedure is not efcient. In such cases,
derivation of PNECs from acute or chronic effect concentrations is not straightforward.
There is considerable incentive to develop QSARs for aquatic NOEC and/or PNEC but the work in
this eld has only started. The ECETOC report on QSARs (ECETOC, 2003) discusses QSARs for
PNEC and lists a number of possible advantages compared with current practice and recommends
further research. QSAR for setting water quality objectives is a related issue discussed by Vighi et
al. (2001). NOEC and/or PNEC model development is a priority eld for further research of QSARs
with applicability in the WFD.
End-point gaps. As noted in this study and by others, e.g. Schultz et al. (2003), there are gaps in
QSAR toxicity model availability, both with respect to chemical substance groups within some
end-points and with respect to availability of models for certain end-points. Few QSARs available
are valid for non-organic chemicals (Comber et al., 2003) and also the validity for metallo-organic
chemicals is limited.
Most of the QSAR work has been devoted to freshwater organisms. There are very few QSARs for
toxicity to estuarine and marine organisms and their quality is generally lower than for freshwater
organisms (ECETOC, 2003, Comber et al., 2003). The same is true for sediment-dwelling organisms.
The need for development of new QSARs here is evident as is for example noted in ECETOC
(1989). QSARs cannot be used for estimation of chronic toxic effects in an aquatic environment
and toxicity to sediment-living organisms today. A signicant obstacle to further development in
these elds is the lack of databases with reference toxicity data.
Approximately 70% of all industrial chemicals are estimated to act acutely via non-polar or polar
narcosis. These mechanisms are also the ones for which most models exist. Non-polar narcosis can
in general be modelled based on log KOW only for individual groups of chemicals. Naturally, for
models covering diverse sets of chemicals, more descriptors are necessary. A remaining challenge
is to model acute and chronic effects of chemicals whose toxicity is elicited through other
mechanisms (covalent binding, receptor interaction etc.; Bradbury et al., 2003).
Antagonistic and synergistic effects. All methods discussed in this report focus on discrete
chemicals and to not account for additive, synergistic or antagonistic effects. This is a signicant
problem for practical use of QSARs in a WFD perspective.
Mode of action based QSARs, however, open a possibility in this direction by allowing the mode
of action to be identied. For compounds acting via the narcosis mode of action, concentrationaddition, a response is often exhibited but for reactive chemicals this is only true for chemicals
having the same target site (Escher and Hermens, 2002).
Some initial QSAR work in this direction has been carried out by Vighi et al. (2003). Further
testing of this approach would be an interesting area for further research.
188 |
Environmental fate
Fate models and the WFD. Mackay et al. (2003) suggest that back-tracking of models should be
used for risk assessment of chemicals in cases where emissions are uncertain or unknown. The
approach is also potentially useful in the context of the WFD. The load (emission) estimates are
often very uncertain but if a PNEC (or similar) concentration from a QSAR model can be used as
a starting point for reverse calculation by a fugacity model. The calculation (which will probably
be of a trial-and-error type) produces an estimate of the critical load that would give an effect on
the organism for which the PNEC is valid. It is then usually feasible to see if the actual loads are
of this magnitude or much smaller. This enables an investigation of which substances that could
be responsible for an observed ecological effect, even in the absence of analytical data (i.e.
environmental concentrations). It could also indicate how much the loads have to be decreased
to lower the concentration of the substance below the PNEC.
End-point gaps. For vapour pressure and water solubility there exists available and well-validated
models covering diverse chemicals that can be used to predict these properties. As noted above,
QSAR estimated melting points can only be recommended for screening purposes (at best). This
failure derives, in part, from ignoring the effects of symmetry in the molecule (Lyman, 1985).
Boiling points are better predicted by existing models but one should be aware of the magnitude
of the error when using these estimates further.
The water-octanol partition coefcient, log KOW, is the most studied of all QSAR end points and a
number of useful models implemented in software exist. Log KOW is also the most common descriptor
for QSARs for other end-points, e.g. bioaccumulation, and sediment-water partitioning. Water-air
partitioning coefcients, most commonly Henrys law constants, are predicted with lower relative
accuracy but available models still give acceptable accuracy for many applications.
Comber et al. (2003) point out the need for improvement of existing models for soil-water
partitioning and sediment-water partitioning. The most likely area to further increase the
usefulness of QSARs for soil and sediment sorption is not through improved QSAR models for
organic carbon normalised partition coefcients, KOC, but through improved understanding of the
sorption process and inclusion of other sediment properties than organic carbon content. Abiotic
aquatic degradation (photolysis, hydrolysis) is poorly covered by existing models as noted in this
study and by others (Comber et al., 2003; ECETOC, 2003).
The QSARs for biodegradation are primarily of classication type while the required input to fate
models, e.g. EUSES, is often quantitative. Thus there is a need for new QSARs for biodegradation
half-lives as noted in this study and by others (Comber et al., 2003; ECETOC, 2003). It should be
noted however that several factors, e.g. the multitude of degradation mechanisms and inaccurate
reference data, could be expected to make QSAR modelling difcult for this end-point. Bioconcentration
factors can be approximately predicted by QSAR models. The need to account for metabolism is
evident and is a weak point of existing models. There are no models available for bioaccumulation.
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10.1 Introduction
The development of new technologies and particularly the genomic revolution has the potential
to completely change the way we address the actions of chemicals and other environmental
stressors on biological systems. To study the effects of environmental contaminants the quite
general concept of biomarkers has been extensively used in the past. According to the National
Academy of Sciences of the USA a biomarker is an indicator signaling events in biological
systems or samples. From a classication point of view there are three broad types of molecular
biomarkers in the eld of environmental toxicology: biomarkers of exposure, biomarkers of effect,
and biomarkers of susceptibility.
Biomarkers of exposure are methods that directly quantify the internal concentration of a given
chemical or metabolites and they are usually applied early in the exposure-disease pathway.
These kinds of markers are very useful for epidemiologists because they allow an accurate
correlation between external and internal dose of an environmental agent. Biomarkers of effect
detect functional changes in the biological system under analyses. This second class of biomarkers
is particularly useful to predict the ultimate outcome of exposure; in particular early markers of
effect can be used to identify populations at risk. Of all the individuals exposed to certain
contaminants only a subclass will in the end develop a disease. The individual susceptibility
depends, in a very complex way, on genetic and environmental factors. These factors include
single nucleotide polymorhisms, age, diet, occupation, and lifestyle.
An ideal molecular biomarker should have several characteristics: highly accurate and reproducible,
specic and sensitive, should provide a plausible biological mechanism for the mode of action, should
be based on a high-troughoutput method of measurements. However, not many biomarkers meet all
the above criteria. One of the best examples is biomarker of exposure to aatoxin. In both animal
models and human studies, DNA adduct level correlates with known external dose of aatoxin and
thus supports the strong epidemiological link between adduct level and risk of liver cancer. A urinary
metabolite of the aatoxin DNA adducts is also used as a quantitative biomarker of exposure.
This chapter reviews the use of Real Time Quantitative PCR, and related methods, in the discovery
and testing of new molecular biomarkers. The chapter focuses on the recent application of
genome-based technologies that propose to apply both mRNA and protein expression technologies
to study chemical effects in biological systems. A common theme of all these techniques is the
objective to develop specic signatures, both at the gene or protein expression level, of exposure
to chemicals and environmental stressors in general. The pattern of gene expression or protein
expression changes induced upon exposure to a chemical both in vitro (Burczynski et al., 2000;
Waring et al., 2001) or in vivo (Hamadeh et al., 2002) would form a sort of genetic signature.
The development of such gene or protein expression signatures would allow a fast screening of
unknown or suspected toxicants based on their similarity to known toxicants.
194 |
195
Polymerization
5
3
5
Forward
primer
Q
Probe
Strand displacement
Reverse
primer
Q
3
5
3
5
Cleavage
5
3
5
5
3
5
Q
3
5
3
5
Polymerization
completed
5
3
5
5
3
5
Q
3
5
3
5
Figure 10.1 TaqMan assay. The RT-PCR reaction exploits the 5 nuclease activity of AmpliTaq Gold DNA
polymerase to cleave a TaqMan probe during the PCR. The Taqman probe contains a reporter dye at 5 end
(R) and a quencher (Q) dye at 3. During the rst step, the primers and the probe anneal at specic target,
and the polymerization starts. During the extension the probe is displaced and cleaved by the exonuclease
activity 5-3. The cleavage of the probe separates the reporter dye from the quencher, resulting in
increased uorescence of the reporter. Accumulation of the PCR products is detected directly by monitoring
the increase in uorescence of the reporter. When the probe is intact, the proximity of the reporter dye to
the quencher results in suppression of the uorescence emission primarily by Foerster-type energy transfer.
with a Minor Groove Binder (MGB) at 3end, thus allowing a tighter binding to the sequence. In
the reaction the probe was labeled with the uorescence dye FAM (6- carboxyuorescein). The
template, the cDNA (the total RNA reverse transcribed to a DNA copy) was diluted up to a few
micrograms. Considering that the mRNA is just 1-2% of the total RNA, the sensitivity of this
technique allows the detection of just a few copies of the gene. Indeed the RT-PCR is extreme
sensitive, it is able to detect less than ve copies of poorly expressed RNA, reveling very small
changes (Bustin, 2000).
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2500
Rn
2000
1500
1000
5000 E-1
10
15
20
Cycle
25
30
35
40
Figure 10.2 Amplication plot. Exponential amplication of TDH3 amplied using TaqMan MGB probe assay.
The reporter dye of the probe is at 5end FAM (6- carboxyuorescin) and at 3end a quencher dye non-orescent
with a Minor Groove Binder (MGB) which increases the binding efciency. The cDNA template was a dilution
series showing different Ct (cycle threshold indicating the rst detection of the TDH3 PCR product) while Rn
represents the uorescence signal. The PCR reaction was performed in triplicate for each cDNA sample.
197
are examined comparing the PCR products only in this range. In order to characterise the hormonal
responsiveness of the three genes: vitellogenin (vtg), estrogen receptor (ER ) and ZP2, adult male
zebrash were exposed to synthetic estrogen 17-ethinylestradiol in a time-dose dependent manner
and the mRNA expression level from liver and gonads was measured. Their study showed Real Time
PCR to be a very sensitive method. Especially for vtg and ER , they were able to detect the presence
of the 17-ethinylestradiol at very low concentration and at short exposure time. In fact the LOEC
(Low Observed Effect Concentration) was 2.5 ng/l for both the biomarkers which lies within the
range of ethinylestradiol concentrations measured in wastewater efuent (Larson et al., 1999).
Galay-Burgos et al., (2003) have described well how Real Time PCR can be applied to assess
exposure to contaminants and how it is possible to differentiate between the effects of different
chemicals. They monitored the expression changes of two selected biomarkers in the earthworm
(Lumbricus rubellus) on control or cadmium-copper spiked soils. They quantied the changes in
the expression of gene encoding for the Methallothionein isoform 2 (MT-2) protein and for the
ribosomal subunit (MLRS) against the internal control, the gene -actin (Kammenga et al., 2000).
The reliability of the assay was demonstrated by the fact that there were no failed reactions of any
of the measured transcripts. The assay reproducibility was also good since they could detect very
low variability from the same transcripts among the experiments.
Rees and Li (2004) developed a RT-PCR assay to monitor the expression changes of CYP1A in the
liver of three salmonid species induced upon -naphtoavone (BNF) exposure. CYP1A or
Cytochromes P4501A constitute a protein family associated with the detoxication of organic
compounds. These compounds induce the CYP1A gene in several tissues of many different shes
(Huuskonen et al., 1998; Levine and Oris 1999). Consequently, the CYP1A changes have been
used as biomarkers for contaminant exposure in sh populations (Cousinou et al., 2000). In the
paper they described the set up of the Real Time PCR assay using the TaqMan probe system. They
designed a primer/probe set to amplify only the CYP1 family and not other P450 (as CYP2 or
CYP3). In addition from the alignment of the known CYP1A sequence from the three salmonid
species, they could identify a conserved sequence to get a highly specic amplication and taking
this advantage to carry the PCR in the same conditions for different species. Furthermore, they
showed the high sensitivity of the assay, measuring CYP1A mRNA expression level down to 1000
transcripts according to the standard curve.
Real Time Quantitative PCR has also been applied to conrm the gene expression changes
obtained by microarray as described by Williams et al., (2003; see Microarray section). They could
compare the expression changes observed in the microarray and conrm the differences giving
condence of the high sensitivity of the two systems.
198 |
changes it elicits both in vitro (Burczynski et al., 2000; Waring et al., 2001) or in vivo (Hamadeh
et al., 2002). The development of such gene expression signatures would allow a fast screening
of unknown or suspected toxicants based on their similarity to known toxicants.
The development of high quality, commercially available, expression arrays has allowed gene
array technology to become a standard tool in molecular toxicology. With this technology cells or
tissues are exposed to toxicants and then gene expression is measured by collecting mRNA,
converting mRNA to labeled cDNA, hybridizing it to the cDNA array, staining it with an appropriate
dye, and visualizing the hybridized genes using a uorometer (Schena et al., 1995; DeRisi et al.,
1996; Lashkari et al., 1997; see Figure 10.3). The raw data are analysed using bioinformatics
software and databases. The aim is to obtain meaningful biological information such as patterns
of relative induction/repression levels of gene expression, participation in biochemical pathways,
and (in the most favorable cases) genetic signatures.
mRNA
mRNA
labelling
labelling
cDNA
cDNA
Hybridize, wash
and scan
Hybridize, wash
and scan
mix
Hybridize and wash
Superimpose
Repressed gene
Repressed gene
Activated gene
Activated gene
Figure 10.3 Gene expression analyses by microarray. a) One-color expression analysis uses a single
uorescent label and two arrays to generate expression proles for two cell or tissue samples (test and
reference samples). Activated and repressed genes are obtained by superimposing images obtained by
the two arrays. b) Two-color expression analysis uses two different uorescent labels and a single array
to generate expression proles for the test and reference samples. Activated and repressed genes are
obtained by superimposing images generated in different channels on a single array. In both cases, the
monochrome images from the scanner are imported into software in which the images are pseudo-colored
and merged. Data is viewed as a normalized ratio in which signicant deviation from 1 (no change) are
indicative of increased (> 1) or decreased (<1) level of gene expression relative to the reference sample.
199
The possibility of analysing the effect of chemicals and environmental stressors on a large number
of genes in a single experiment has led to the development of the eld of toxicogenomics. Proponents
of toxicogenomics propose to apply both mRNA and protein expression technology to study chemical
effects in biological systems (Afshari et al., 1999; Lovett 2000). The availability of the (almost)
complete human genome and several other organisms (see http://www.ncbi.nlm.nih.gov/
Genomes/index.html for a list of nished and ongoing projects) allows the application of microarray
technology to several model organisms (from bacteria, to yeast, to sh) and mammalian cell lines.
To expand the application of microarray technology to toxicology several national and international
initiatives have been started in order to obtain a better standardisation and harmonisation of the
technology. In fact, one of the early concerns has been how to properly compare experiments that
use a wide variety of commercially available and proprietary platforms, protocols, instrumentation,
and analysis methods.
In the United States the National Institute of Environmental Health Sciences (NIEHS) has created
the National Center for Toxicogenomics (NCT) to provide a reference system of genome-wide gene
expression data and to develop a knowledge-base of chemical effects in biological systems (Tennant,
2002). The NCT has conducted some proof-of-principle experiments to establish signature proles
and to link the pattern of altered gene expression to specic parameters of conventional indices of
toxicity (Bartosiewicz et al., 2001; Bulera et al., 2001; Hamadeh et al., 2002). These studies have
shown that it is possible to identify signature of expressed gene patterns (Tennant, 2002).
The Health and Environmental Sciences Institute (HESI) of the International Life Sciences Institute
(ILSI) has coordinated an international study, involving more than thirty pharmaceutical
companies, to evaluate the harmonization of gene expression data and analyses (Pennie et al.,
2004). In the ILSI Genomic Project common pools of RNA were analysed in more than 30 different
laboratories on both similar and different technical platforms. Overviews of the design and
objectives of the experimental program and more technical articles were published in the minimonograph Application of Genomics to Mechanism-Based Risk Assessment published in
Environmental Health Perspectives, 2004, vol. 112, number 4. For example, Amin et al., (2004)
identied gene markers of renal toxicity, Thompson et al., (2004) identied markers of cis-platin
nephrotoxocity, while three groups reported an overview on the inter-laboratory collaboration to
evaluate the effects of nephrotoxicants (Kramer et al., 2004), genotoxic chemicals (Newton et al.,
2004), and hepatotoxicants (Ulrich et al., 2004) on gene expression.
The experimental program detailed in Pennie et al., (2004) has shown that: a) patterns of gene
expression relating to biological pathways are robust enough to allow insight into mechanisms of
toxicity; b) gene expression data can provide meaningful information on the physical location of
the toxicity; c) dose-dependent changes can be observed; and d) concerns about oversensitivity of
the technology may be unfounded.
200 |
array (Southern, 2000). It was only a small step to lter-based screening of clone libraries, which
introduced a one to one correspondence between clone and hybridization signals (Grunstein and
Hogness, 1975). The next advance has been the use of gridded libraries, stored in microtiter
plates, and stamped onto lters in xed position. With this system each clone could be uniquely
identied and information about it accumulated. Several groups have explored expression analysis
by hybridizing mRNA to cDNA libraries gridded on nylon lters. The subsequent explosion of array
technologies has been sparked by two key innovations. The rst has been the use of non porous
solid support, such as a glass, which has facilitated miniaturization and uorescence-hybridization
detection (Schena et al., 1995; Lockhart et al., 1996; Schena et al., 1996). The second critical
innovation has been the development of methods for high-density spatial synthesis of
oligonucleotide which allows the analysis of thousands of genes at the same time.
Recently, a signicant technical achievement was obtained by producing arrays with more than
250,000 oligonucleotide probes or 10,000 different cDNAs per square centimeter. DNA microarrays
are fabricated by high speed robotics, generally on glass. Since the DNA cannot bind directly to the
glass, the glass is rst treated with silane to covalently attach reactive amine, aldehyde, or epoxide
groups. Such surfaces allow stable attachment of DNA, proteins, and other molecules.
The nucleic acid microarrays use short oligonucleotide (15-25 nt), long oligonucleotide (50-120
nt) and PCR-amplied cDNAs (100-3,000 bp) as array elements. The short oligonucleotide is
primarily used for detection of single nucleotide polymorphism (SNPs). Because this application
requires the discrimination of only one mismatch, the presence of a short oligonucleotide
maximises the destabilisation caused by mispairing (Lockhart et al., 1996). On the other hand, the
PCR-amplied cDNAs produce strong signals and high specicity (DeRisi et al., 1996). The cDNAs
elements are obtained readily from cDNA libraries, and are typically used for organisms for which
the available genomic sequence is limited. The long nucleotides offer strong hybridization signal,
good specicity, unambiguous sample identication and affordability (Schena et al., 1998;
Hughes et al., 2000; Kane et al., 2000).
201
showed an additive effect for multiple stressors. Similar results were found when using different
stressors like temperature shock, amino acid starvation, nitrogen source depletion (Gasch et al.,
2000) and cadmium (Momose and Iwahashi, 2001). The same approach has been used to
characterise the alteration of gene expression in yeast induced by the pesticide thiuram (Kitagawa
et al., 2002). The results obtained for stress response in yeast will be likely to provide a reference
frame for similar experiments that use more complex organisms.
This methodology has been recently applied to a typical model organism: zebrash, to understand
responses to endocrine modulators (Hoyt et al., 2003). Hoyt and coworkers used a microarray
approach to study the response of zebrash embryos exposed in vitro to the environmental
contaminant 4-nonylphenol (4NP). Using a custom microarray with 230 genes they were able to
identify a set of nine genes associated with the function of estrogen response that are indicative
of embryo exposure to 4NP, even at low concentrations. The application of gene expression
proles is not limited to model organisms for which the complete (or almost complete genome) is
available. Several strategies are available to apply a genomic approach in ecotoxicology even
before genomes are completed.
One approach consists in heterologous hydridization. In fact, due to the length of the probes,
cDNA microarrays can be used in heterologous hydridizations across strains and relatively closely
related species as long as sequence divergence is limited for a given gene (Rise et al., 2004a,b).
For example, this approach has been used to study the molecular basis of traits like hibernation
not present in model species (Hittel and Storey, 2001). More recently heterologous hybridization
has been used to study gene expression proling across a wide range of different species of
African cichlid sh (Renn et al., 2004).
Another possible approach consists of identifying stress-induced genes using special techniques
based on polymerase chain reaction (PCR), such as differential display PCR (DD PCR), suppressive
subtractive hybridisation (SSH PCR), and representational difference analyses (RDA). The
application of these techniques to ecotoxicology has been reviewed by Snell et al., (2003). Gracey
et al., (2001) have used cDNA microarrays to identify hypoxia-induced genes in a non model sh
for which sequence data were unavailable. Their analyses revealed that although some changes
in gene expression mirror the changes that take place in mammals, novel genes are differentially
expressed in sh and that there are tissue-specic patterns of gene expression during hypoxia.
Larkin et al., (2003) have described an expression proling model system for endocrine-disrupting
compounds (EDCs) that mimic estrogens. The team created a gene array by cloning 30 genes
from sheepshead minnows. The genes had previously been identied by differential display
reverse transcriptase-polymerase chain reaction, a method that screens thousands of RNA
messages to identify genes that are turned on or off by specic treatments. They treated the sh
with a constant concentration of weak and strong environmental estrogens and then analysed
which genes were differentially expressed in the livers of treated and control sh. They found
genes that were upregulated by all the test compounds while other genes were specic for a
single compound. Exposure to different concentrations of the strong estrogen 17-ethynyl
estradiol revealed that their microarray is dose-sensitive and that exposure thresholds vary for
different genes. A similar approach has been used to identify alterations in gene expression due
to exposure to androgen hormones in largemouth bass sh (Blum et al., 2004).
202 |
Williams et al., (2003) used a cDNA microarray-based approach to analyse the expression level
changes of recognised biomarkers in a relevant sh species: European ounder (P. esus). They
arrayed 160 genes, among which 110 were already known in the literature as biomarkers for sh
and mammalian toxic response. Five adult male and ve adult feral female P. esus were caught
from Tyane (polluted) and Alde (unpolluted) estuaries. They observed that eleven genes were
expressed differently between the Tyane and Alde males. Such differences were not statistically
signicant in females due to the inter-individual variations. In fact the vitellogenin levels differed
radically among the female sh suggesting that their reproductive cycles were at different stages.
Very recently, microarray analyses have also been successfully applied to identify molecular
markers of pathogen infection in salmonids (Rise et al., 2004a,b).
2
Condition A
Solubilize proteins
from cells
pH
203
10
Reduction
and alkylation
Condition B
Isoelectric focusing on
narrow- or broad-range pl strips
(rst dimension)
SDS-PAGE
(second dimension)
Staining
1. Silver
2. Coomassie
3. Fluorescent
4. Autoradiography
200
100
70
45
20
Mass spectrometric
identication of spots
Excision of spots of interest
Condition A Condition B
Image analysis
Figure 10.4 Schematic picture of the two-dimensional gel electrophoresis approach to proteomics. Cells (or
tissue) derived from two different conditions: A and B, are collected and the proteins solubilised with an
appropriate buffer. The crude protein mixture is then separated based on the different isoelectric point of
the proteins (rst dimension). Then the proteins are reduced and applied to a second dimension SDSPAGE gel where they are separated on the basis of protein size. The gels are then xed and the proteins
visualised by silver staining. After staining, the resulting protein spots are recorded and quantied with
image analyses software. The spots of interest are then excised and analysed with mass spectrometry.
charge (isoelectric focusing) and then by protein mass (PAGE). In some experiments, before the
gels are run, the proteins are tagged with uorescent markers to allow later detection. In other
cases, the proteins are chemically stained after separation. The end result is a series of spots and
smears that represent a portion of the proteins in the sample. With this technique a thousand
protein spots are readily visible on a single gel (Blomberg et al., 1995) and the separation of up
to 10,000 proteins has been reported (Klose and Kobalz, 1995).
Even though whole cell analyses still relies primarily on the use of 2DE as its primary separation
technique, it is being replaced by multidimensional HPLC. In a typical application, microscale twodimensional liquid chromatography (2DLC) is coupled with electrospray ionization (ESI) tandem
mass spectrometry (MS/MS) (Liu et al., 2002; Aebersold and Mann 2003). This combination of
powerful separation and identication techniques has allowed, for example, a very important
breakthrough in the understanding of the Plasmodium falciparum life cycle (Florens et al., 2002).
The identication of the individual proteins present in the system under analysis is done using mass
spectrometry (MS). A mass spectrometer discriminates between chemical compounds by separating
molecular ions according to the mass-to-charge (m/z) ratio, allowing the determination of molecular
mass. The key improvement that has allowed the use of MS for the identication of proteins has been
the development of soft methods of ionization such as matrix-assisted laser desorption ionization
204
(MALDI) and electrospray ionization (ESI). These two methods allow the ionization of large
biomolecules such as proteins with very little or no fragmentation (thus the term soft ionization).
The third key part of the proteomics technique is the availability of a large number of fully
sequenced genome that allows the peptide mass ngerprinting (Sagliocco et al., 1996; Shevchenko
et al., 1996). In this method the protein to identify is subjected to proteolytic digestion with a
preotease (usually trypsin). The masses of the resulting peptides are acquired by mass spectrometry
to give an experimental peptide ngerprint. This experimental ngerprint is then compared with
all the predicted peptide ngerprint of that organism available in the complete proteome
database. A protein that has the most theoretical peptide fragments in accordance with the
experimental data is identied as the best matched protein.
Early applications of proteomics have focused on the differences, at the protein level, between
normal and cancerous cells. A study compared the proteome of normal human luminal and
myoepithelial breast cells using immunopuried cell populations. It detected 170 spots with a
twofold difference in expression levels (Page et al., 1999) and identied 52 of them. Several
groups have probed two-dimensional gels of proteins from allergy-causing organisms using
antibodies derived from allergic patients (Breitenbach et al., 1996; Sander et al., 1998). Very
recently the technique has been used to follow the time course of the phosphotyrosine dependent
signaling network. Blagoev et al., (2004) grew individual cell cultures in medium containing
isotope-labeled arginine variants, and then stimulated each with EGF for different lengths of time.
Tyrosine-phosphorylated proteins were afnity puried and subjected to mass spectrometry.
205
10.9 Summary
Gene expression and protein expression proling represent a unique way of characterising how
cells and organisms adapt to changes in the external environment. The measurements of such
changes upon exposure to a chemical can be used both to provide information about the
mechanism of action of toxicants and also to form a sort of signature for the identication of
toxic products. Several key technical advances have allowed proteomics to become an established
discipline in system biology and in the biomedical sector. At the same time the development of
high quality, commercially available, gene arrays has allowed this technology to become a
standard tool in molecular toxicology. Several national and international initiatives have provided
the proof-of-principle tests for the application of gene expression and proteomics to the study of
toxicology of new and existing chemical compounds. In the last few years the eld has progressed
from evaluating the potential of the technologies to illustrating the practical use of gene
expression proling and proteomics in toxicology.
The application of the above technologies to ecotoxicology is at an early stage, due mainly to
more complex problems at hand, and to the many more variables involved in analysing the status
of natural populations in a real ecosystem rather than in a laboratory environment. Nevertheless,
signicant studies have been carried out to study responses to environmental stressors in both
model and non-model organisms. It can be easily predicted that the development of stressorsspecic signatures in ecotoxicology will have a similar potential as the toxicant signatures in
toxicology studies.
One of the best ways to advance the eld is probably to focus on more precise objectives that have
been neatly outlined in a recent paper by Snell et al., (2003): identication of conserved genes
that are up-regulated in response to toxicant exposure; how these gene-expression proles can be
used to diagnose stressors; and determination of which genes are most informative to incorporate
into stress gene arrays.
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Combined pressures
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11.1 Introduction
The purpose of this chapter is the description of relationships between a combination of pressures
coming from human activities (agriculture, urbanisation, etc.) and ecological status of European
rivers, with a large scale approach. However, across Europe, the natural and human geographical
contexts are very diverse, and thus the relationship between anthropogenic pressures and
ecological status may vary according to the sensitivity of river ecosystems and combinations of
pressures. A regional framework related to the dominant ecological processes is useful to properly
identify the strength of the pressures-impacts relationships.
This chapter is a review of the relevant literature on this kind of models, linking pressures and river
ecological status (through biological indicators) at large scales, with emphasis on the possible
variability related to the geographical context. In a recent, very clear and comprehensive review,
Allan (2004) addressed similar questions and most of our ndings are consistent with his
conclusions.
WFD requirements
The Water Framework Directive (WFD) requires the identication of signicant anthropogenic
pressures and the assessment of their impacts on water bodies (Annex II, WFD). These ecological
impacts are not only determined by clearly identied point sources discharges, but also by series
of complex human inuences including diffuse pollution, alteration of water and sediment
regimes, hydro-morphological changes, connectivity breaks etc. (Borchardt and Richter, 2003).
Ecological quality is integrating all pressures and showing the overall status of the ecosystem.
(EEA, 2003). In most cases various pressures are acting simultaneously, and managers must
dene a hierarchy amongst these to identify priority actions. Moreover, these pressures are not
evenly distributed on the territory, and decisions makers have to decide where to act in priority.
Finally, pressures are generated by different kinds of human activities, and integrated policies to
restore river ecosystems must be tailored towards whole socio-economical structures, such as
agricultural sectors, industry, urban areas, etc. This means that an integrated approach and policy
should include possibilities to have differentiated measures according to the nature of the
different waterbodies and to the socio-economic conditions within the catchment.
214
First, the criteria to identify and assess pressures must be based on available data. But many
pressures are difcult to identify and measure, especially when working in large territories. In most
cases, we have not the same level of information upon the various kinds of pressures, such as
chemical and hydro-morphological, point sources or diffuse, at the local or basin scale. For this
reason, it is often necessary to rise up at the level of the driving forces to get spatially homogeneous
information (Figure 11.1). For example, it is very difcult to determine in a large basin the amount
of pesticides and nutrients rejected, the sediment yield due to erosion, the degree of river
channelization etc., but we have access to the percentage of land dedicated to one kind of
agriculture that generates these pressures.
Second, in large spatial contexts, the inuence of scales when studying ecological processes is a
key issue (Allan, 2004). One important problem is the upscaling of ecological relationships: how
a model developed at a local scale can be safely extrapolated to larger areas? Another one is
related to the interactions between natural characteristics that determine the sensitivity of river
ecosystems and anthropogenic alterations: has a given pressure the same impact in different
regions?
To address these questions, it is necessary to study pressure-impact relationships in geographically
homogeneous areas, in order to identify the relative inuence of human and natural drivers of
ecosystem responses (Allan, 2004). The proper way for doing that is to work at the level of hydroecoregions, which are considered homogeneous with respect to the natural factors (geology,
relief, climate) that control the functioning of the aquatic ecosystems (Wasson et al., 2002).
Driving forces
Pressures
Impact
215
Status
Abiotic parameters
Population
density
urbanization
Agriculture
Land use
Pollution inputs
point
non point
Pollution
Organic (MO)
Nutrients N,P
Toxics, acidication
Tourism
Invertebrates
Fish
Industries
Water uses
energy
transport
Bioindicators
Dams
Abstraction
Derivation
Channelization
Physical alteration
Diatoms
Hydrology
Morphology
Figure 11.1 Possible indicators that could be used in the development of pressure- impact models.
However, when studying the large scale effects of combined pressures, it is often necessary to use data
from the level of the driving forces, in order to get spatially homogeneous indicator data.
The biological effects of agriculture have been noted by several authors: decrease in the number
of species (taxa richness) and abundance of sh and invertebrates, shift in communities
composition for algae (Bis et al., 2000; Cuffney et al., 2000).
Urbanization. The primary impacts of urbanization are related to direct point sources pollution,
due to raw or treated sewage inputs. Pollution problems are well known by the managers, and
most of the nancial investments are dedicated to reduce sewage pollution. However, many others
pressures are related to urban areas (Allan, 2004; Walsh, 2000). Housing, roads and other
infrastructures constitute impervious surfaces. Increased impervious area may result in altered
hydrological regimes: changes in timing, frequency, duration and magnitude of ood events
(Cormier et al., 2000), with hydro-morphological and biological consequences. Untreated storm
water runoff may cause also acute problems of organic or toxic pollution. And nally, many
channelization works are dedicated to the ood protection of urbanized areas.
Other driving forces. More specic problems are related to large industries, energy production,
navigation, tourism, etc. However these problems are generally well known by the managers, and
depend on local specic measures, or will induce the designation of heavily modied water bodies
with adapted environmental objectives. These pressures (often concerning large rivers) are not
easily integrated in a large scale view, and deserve a more targeted approach.
In most cases, it is impossible to get precise information on these multiple pressures at large
scales. However, analysing in a rst approach the relative impacts of agriculture and urbanization
can provide to the decision makers, at the district or state level, useful information for the choice
of management priorities.
216 |
217
In one of the pioneer works, Steedman (1988) evidenced positive relationships between the sh
communities (IBI) and the percentage of forest in the basin, the proportion of channel with
riparian forest, and a strong negative impact of watershed urbanization. He emphasised also the
need of more detailed evaluation of agricultural land use, and streamside vegetation to improve
predictive models. As stated by Allan (2004), most of these issues are still open, and the challenge
for the research is to shift from descriptive relationships to predictive models, usable for the
denition of management policies.
218 |
219
processes. Bryce and Clarke (1996) linked landscape-level ecoregions within a basin to bridge the gap
between stream habitat and state-level ecoregions classications. Boulton (1999) reviewed the
denitions for the concept of river health, and the indicators that were chosen for different scales. The
large scale approach is also addressed by Naiman and Turner (2000), who recognised the need for
improved understanding of the processes at the watershed and landscape levels.
220 |
Pressures
(land cover)
Creation and validation of a
predictive decision tree from
the le stations-pressures
Biological
stations
Pressures
(land cover)
Articialised < X%
Yes
No
Application of the
predictive model to
the pressure of the
subcatchments
Subcatchments
External
validation
1.0
0.8
0.6
0.4
0.2
0.0
G/B
W5 B/G
Articialised < Y%
No
Yes
Mapping the
probalility of
good/bad status
Probable GS
Probable BS
Figure 11.2 Pressure-impact models: methodological approach for the spatial extrapolation.
Present probability of good/bad ecological status based on decision tree models at the sub-catchment
scale. G = good status; B = Bad status; W = well predicted; G/B = predicted good/observed bad;
B/G = predicted bad/observed good. See text for details.
From these results, predictive outcomes are used to map the present probability of good ecological
status, based on the IBGN index, for the main branch of each subcatchment (Figure 11.3).
The whole process is repeated using a slightly higher good status boundary to identify
borderline situations, i.e. the sub-catchments that are at the edge of the present good status
denition (Figure 11.3).
Diagnostic of dominant driving forces with Partial Least Square regression models. The
objective here is to run an explicative analysis to identify the categories of land cover that have the
strongest negative or positive correlation with the EQR value of the IBGN index. For each IBGN site,
the land cover is evaluated in the corresponding catchment and in a 3 km long riparian buffer. The
model used is a Partial Least Square regression (PLS; deJong, 1993; Tenenhaus, 1998).
An example of the model results for the whole France a given in Figure 11.4. The results clearly
indicate that the constructed areas in the catchment are impacting most, whereas forested and
natural areas and the low impact agriculture (pastures) in the riparian buffer have the most
positive effect on the IBGN. Further models have been run in the level of the hydro-ecoregions
using more precise land use categories in order to provide more precise diagnostics relevant for
the hydro-ecogerion scale.
0.8
FRANCE
MEDITER.
TYPE
HER 5
HER 9,
20, 12
0.4
221
0.0
Borderline situation
0.8
0.4
0.0
0.8
0.4
0.0
HER 1
AND 2
G/B
HER 3,
4, 21,
17, 19
W
B/G
G/B
B/G
Figure 11.3 Map of the present probability of good/bad status and borderline situations at the
subcatchment scale, from pressure/impact models relating invertebrate index (EQR-IBGN) to land cover
(CORINE). Six different models have been elaborated for ve groups of hydro-ecoregions and for the whole
France. On the right, external validation (see gure 11.2 for legend).
Station
catchment
Built up areas
High impact agriculture
(arable land)
Low impact agriculture
(pastures...)
Forest and natural areas
Station
riparian
buffer
Built up areas
High impact agriculture
(arable land)
Low impact agriculture
(pastures...)
Forest and natural areas
Figure 11.4 Results of the PLS regression for France. Cross-validated, R2 = 16.3%. Correlation coefcient
between EQR (IBGN) and land cover (from CORINE Land Cover) of the station catchment and riparian
buffer (analysis on 3640 stations).
11.8 Summary
Despite the strong need, research approaches at the large spatial scale are not well developed.
Due to the traditional focus on one single basin, watershed, or ecoregion, there is a lack of studies
comparing different regions. However, in order to provide tools for large scale decision-making,
especially within the diverse territories in Europe, an regional approach would be very useful to
identify 1) comparable issues even in regions spatially separated and 2) different regional river
222 |
pathologies that should be managed differently even within a country. This would set a coherent
natural framework for monitoring and management of rivers. So far ecoregional scale has not
been widely used in large-scale studies on pressures-impact relationships.
The proportion and the hierarchy of the different driving forces impacting stream ecosystems are
not clear in the light of the papers reviewed. Although the negative effects of agriculture on the
integrity of the stream ecosystems are generally indicated by several studies, there is not sufcient
scientic basis to quantify the degree of impairment, or discriminate the effects from different kinds
of agricultural practises, or to set the thresholds (of % of agricultural land use, for example).
Differences in the methodologies (selection of bioindicators, methods, or models) may be the
reasons that no clear differentiation has been found in several studies, whether the share of
agricultural vs. urban areas could be most impairing activity. This could be also because the
hierarchical relations between the driving forces vary depending on the level and type of development,
or within the ecoregional context. Ecosystems sensitivity, related to the natural characteristics, may
inuence the intensity of the impairment. Due to the covariation of anthropogenic and natural
landscape features (Allan, 2004), natural constraints may determine both ecosystems sensitivity
and land use practices in different regions, thus leading to different regional responses.
However, the key issue is that the national socio-economic context determine the intensity of the
pressures generated by a given land use, as well as the policies adopted to alleviate the impacts.
For example, the same category of agricultural land cover may have different effects in terms of
pollution, sediment yield etc. on water ecosystems, depending if the practices are intensive or
extensive. In the same way, depending on waste-water treatment practises, two urban areas of
same size may not have the same impacts. In this way the treatment practices may increase or
reduce the intensity of the pressures depending on the local, regional or national socio-economical
context. In conclusion, more detailed treatment practices must be introduced in the system to
better understand the relationships between driving forces and pressures.
Treatment
practices
Driving forces
Pressures
The different processes that take place at different spatial scales, like within a riparian corridor vs.
basin scale, need to be understood better (Allan, 2004). It is difcult to conclude which is the
inuence of the local riparian corridor, or the upstream riparian corridor, or the basin or sub-basin
land use conditions on the impacts on the biota at a given site. The review of the results from
previous studies indicate contrasting results; some studies identify landscape-level factors as the
main variables for predicting biological indicators, while others nd no relationships beyond the
local scale measurements. It is not clear whether these discordances are due to the different
anthropogenic factors, natural characteristics, or due to the different methods or indicators used.
Nevertheless, all these factors and scales have to be considered when developing models. The
restoration of river corridors is often seen as the most important action to improve the ecological
status. Still, the actual buffering capacity of riparian areas needs to be properly evaluated.
The same applies with the existence of thresholds in the relations between driving forces and
ecological status. Some managers are wondering if a good ecological status is attainable in
223
heavily urbanized basins, or in intensively cultivated areas. Some of the models indicate threshold
levels, beyond which streams are systematically impaired. A comparison and validation of such
models should be made within the European territory. This is a complicated issue as the different
biological compartments may not have the same response curve to a given pressure. Another
important related question is the feasibility of spatial extrapolation of ecological status on the
basis of land use in water bodies which are not monitored.
In general, it seems that the present knowledge is not sufcient to give clear advice to decision
makers (Allan, 2004). The large scale approaches are relatively recent, so there is a lack of
conceptual models and experiences. Nevertheless, large scale analysis comparing pressure-impact
relationships across different spatial scales, countries, and ecoregions would still be necessary for
the implementation of the WFD in Europe.
11.9 References
Addicott, J.F., J.M. Aho, M.F. Antolin, D.K. Padilla, J.S. Richardson, and D.A. Soluk. 1987. Ecological
neighbourhoods: scaling environmental patterns. Oikos, 49: 340-346
Allan, J.D. 2004. Landscapes and Riverscapes: the inuence of land use on stream ecosystems. Annual
Review of Ecology Evolution Systematic, 35: 257-284
Allan, J.D., D.L. Erickson, and J. Fay. 1997. The inuence of catchment land use on stream integrity across
multiple spatial scales. Freshwater Biology, 37: 149-161
Bis, B., A. Zdanowicz, and M. Zalewski. 2000. Effects of catchment properties on hydrochemistry, habitat
complexity and invertebrate community structure in a lowland river. Hydrobiologia 422: 369-387
Borchardt, D., and S. Richter. 2003. Identication of signicant pressures and impacts upon receiving waters.
Water Science and Technology, 48: 33-38
Boulton, A.J. 1999. An overview of river health assessment: philosophies, practice, problems and prognosis.
Freshwater Biology, 41: 469-479
Breiman, L., J.H. Friedman, R.A. Olshen and C.J. Stone. 1984. Classication and regression trees. Wadsworth
International Group, Belmont, California, USA
Bryce, S.A., and S.E. Clarke. 1996. Landscape-level ecological regions: linking state-level ecoregion frameworks
with stream habitat classications. Environmental Management 20: 297-311
Cormier, S.M., M. Smith, S. Norton, and T. Neiheisel. 2000. Assessing ecological risk in watersheds: A case
study of problem formulation in the Big Darby Creek watershed, Ohio, USA. Environmental Toxicology and
Chemistry, 19: 1082-1096
Cuffney, T.F., M.R. Meador, S.D. Porter, and M.E. Gurtz. 2000. Responses of physical, chemical, and biological
indicators of water quality to a gradient of agricultural land use in the Yakima River Basin, Washington.
Environmental Monitoring and Assessment, 64:259-270
deJong S. 1993. SIMPLS: An alternative for partial least squares regression. Chemometrics and Intelligent
Laboratory Systems, 18:251-263
Dovciak, A.L., and J.A. Perry. 2002. In search of effective scales for stream management: Does agroecoregion,
watershed, or their intersection best explain the variance in stream macroinvertebrate communities?
Environmental Management, 30: 365-377
EEA (European Environment Agency). 1991. Europes Environment. The Dobris Report. European Environment
Agency, pp. 676
EEA (European Environment Agency). 2003. Europes water: an indicator-based assessment. Luxembourg:
Ofce for Ofcial Publications of the European Communities. pp. 97
Gergel, S.E., M.G. Turner, J.R. Miller, J.M. Melack and E.H. Stanley. 2002. Landscape indicators of human
impacts to riverine systems. Aquatic Sciences, 64: 118-128.
224 |
Harding, J.S., E.F. Beneld, P.V. Bolstad, G.S. Helfman, and E.B.D. Jones. 1998. Stream biodiversity: the ghost
of land use past. Proceedings of the National Academy of Science USA, 95: 14843-14847
Karr, J.R. 1981. Assessment of biotic integrity using sh communities. Fisheries, 6: 21-27
Lammert, M., and J.D. Allan. 1999. Assessing biotic integrity of streams: Effects of scale in measuring the
inuence of land use/cover and habitat structure on sh and macroinvertebrates. Environmental
Management, 23:257-270
Lange-Bertalot, H. 1979. Pollution tolerance of diatoms as a criterion for water quality estimation. Nova
Hedwigia 64:285-304
Meador, M.R., and R.M. Goldstein. 2003. Assessing water quality at large geographic scales: Relations
among land use, water physicochemistry, riparian condition, and sh community structure. Environmental
Management, 31:504-517
Naiman, R.J., and M.G. Turner. 2000. A future perspective on North Americas freshwater ecosystems.
Ecological Applications, 10:958-970
Pan, Y.D., A. Herlihy, P. Kaufmann, J. Wigington, J. Van Sickle, and T. Moser. 2004. Linkages among land-use,
water quality, physical habitat conditions and lotic diatom assemblages: A multi-spatial scale assessment.
Hydrobiologia 515:59-73
Roth, N.E., J.D. Allan, and D.L. Erickson. 1996. Landscape inuences on stream biotic integrity assessed at
multiple spatial scales. Landscape Ecology, 11:141-156
Roy, A.H., A.D. Rosemond, D.S. Leigh, M.J. Paul, J.B. Wallace. 2003a. Habitat-specic responses of stream
insects to land cover disturbance: biological consequences and monitoring implications. Journal of the
North American Benthological Society 22:292-307
Roy, A.H., A.D. Rosemond, M.J. Paul, D.S. Leigh, and J.B. Wallace. 2003b. Stream macroinvertebrate response
to catchment urbanisation. Georgia, USA. Freshwater Biology, 48:329-346
Sponseller, R.A., E.F. Beneld, and H.M. Valett. 2001. Relationships between land use, spatial scale and
stream macroinvertebrate communities. Freshwater Biology 46:1409-1424
Steedman, R.J. 1988. Modication and assessment of an index of biotic integrity to quantify stream quality
in Southern Ontario. Canadian Journal of Fisheries and Aquatic Science, 45:492-501
Stepenuck, K.F., R.L. Crunkilton, and L.Z. Wang. 2002. Impacts of urban land use on macroinvertebrate communities
in south-eastern Wisconsin streams. Journal of the American Water Resources Association, 38:1041-1051
Stewart, J.S., L. Wang, J. Lyons, J.A. Horwatich, and R. Bannerman. 2001. Inuences of watershed ripariancorridor, and reach-scale characteristics on aquatic biota in agricultural watersheds. Journal of the American
Water Resources Association 37:1475-1487
Tenenhaus, M. 1998. La rgression PLS, thorie et pratique. Technip, Paris
Van Dam, H., A. Mertens, and J. Sinkeldam. 1994. A coded checklist and ecological indicator values of
freshwater diatoms from the Netherlands. Netherlands Journal of Aquatic Ecology 28:117-133
Walser, C.A., and H.L. Bart. 1999. Inuence of agriculture on in-stream habitat and sh community structure
in Piedmont watersheds of the Chattahoochee River System. Ecology of Freshwater Fish 8:237-246
Walsh, C.J. 2000. Urban impacts on the ecology of receiving waters: a framework for assessment, conservation
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across multiple spatial scales. Environmental Management, 28:255-266
Wang, L., and P. Kanehl. 2003. Inuences of watershed urbanization and instream habitat on
macroinvertebrates in cold water. Journal of the American Water Resources Association 39:1181-1196
Wasson, J.G., A. Chandesris, H. Pella, and L. Blanc. 2002. Typology and reference conditions for surface water
bodies in France: the hydro-ecoregion approach. TemaNord, 566:37-41
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mthodologique, modles dextrapolation spatiale et modles de diagnostic de ltat cologique bass sur les
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225
12.1 Introduction
Eutrophication and pollution are both major pressures on aquatic systems that often co-occur.
Studies (Schaaning et al., 1996 and Gunnarson et al., 1996) show that the eutrophication can
inuence the fate of contaminants in the system and that pollutants can affect the response of
ecosystems to nutrients. The interactions between the pressures are highly complex and may
inuence all levels of the ecosystem. The effects of eutrophication and contamination have been
mostly investigated separately in the past and potential interactions were not considered. However,
the reduction/increase of the concentration of only one pressure may alter the fate of the other.
For the prediction of effects of changes in inputs of nutrients, organic matter and contaminants
on the aquatic system, interactive mechanisms that may alter bioavailability and the fate of
contaminants have to be considered.
Two closely connected research programmes investigating interactions between eutrophication
and contamination in aquatic systems were launched in 1995 for a ve-year period. The Swedish
EUCON (Eutrophication and Contaminants in the aquatic environment) project examined
interactive processes between eutrophication and contaminants (selected organic pollutants and
some metals) in marine and freshwater environments. The connected Norwegian strategic
programme MILE (Interaction between contaminants and eutrophication) investigated interactive
processes relating to the benthos and pelagial in the marine environment focussing on selected
heavy metals, metal organic compounds (e.g. TBT), polycyclic aromatic hydrocarbons (PAHs),
polychlorinated biphenyls (PCBs) and pesticides (e.g. DDT).
Interactive mechanisms included both in EUCON, MILE and other combined effect studies were:
biodilution and growth dilution, sedimentation and sediment sequestering, the importance of
lipids, food quality, organism characteristics and food web structure. In this chapter we summarise
the main interactive mechanisms and introduce case studies investigating the responses of biota
to contaminants in systems of different trophic regimes for the pelagial and benthos. Pioneer
models that are capable of simulating chemical fate/effect and food chain accumulation at
varying trophic levels are reviewed in regards to risk assessment and as decision tool for integrative
ecosystem management.
226 |
227
The nature and composition of organic matter is important for the HOC dynamics in water.
The sorption and accumulation of HOCs in phytoplankton are inuenced by a variety of factors:
The binding of lipophilic persistent compounds such as HOCs is related to the amounts
of lipids and their quality in the different algae species (Larsson, 1997 and Skei et al., 2000).
It is believed that the cell wall composition can inuence the initial adsorption of the
pollutant (Skei et al., 2000). The lipid composition of the pelagic community inuences
the uptake of HOCs from water.
Dissolved organic carbon (DOC) matrices inuence the solubility of HOCs (Gjessing and
Berglind, 1981; Hassett and Anderson, 1979 and McCarthy and Jimenez, 1985) and are
crucial for the availability of HOCs in the water to the biota. According to Jonsson et al.
(1996), DOC also has a gluing effect during the aggregation process that facilitates the
formation and/or growth of different particles and colloid types. Taylor et al. (1997) point out
that DOC is a large pool relative to POC in lakes and that changes in DOC caused by changes
in the trophic status can inuence the bioaccumulation of HOCs signicantly.
The importance of DOCs for the distribution and dynamics of many metals (e.g. Pb, Cu, Ni,
Co, Zn, Cd, Fe, Mn and Mg) has been demonstrated in natural sea water. DOC forms
complexes with the metals increasing their solubility and altering the distribution between
the oxidised and reduced form (Jonsson et al., 1996). Frstner and Wittman (1983) mention
that DOCs can inuence the extent to which metals adsorb on particular matter and thereby
affect the stability of colloids that contain metals.
The trophic status of the system impacts on the phytoplankton composition. The biomass of
many eutrophic lakes is dominated by blue-green algae such as Planktothrix, Anabaena and
Apanizomenon (Larsson, 1997). These species contain lower amounts of lipids and posses
different types of cell walls in comparison with diatoms and green algae. Further,
cyanobacteria can be less impacted by zooplankton through food selectively. Therefore, there
may be no signicant biomagnication of HOCs along the pelagic food chain (phytoplanktonzooplankton- sh) through the blue-green algae link (Larsson, 1997). Oligotrophic lakes
normally display a diverse phytoplankton community that is mostly dominated by diatoms
and green algae (Larsson, 1997). Both of these groups contain high amounts of lipids and
may absorb higher concentrations of lipophilic pollutants (Skei et al., 2000).
Larsson et al. (2000) point out that growth rate of phytoplankton can be high in eutrophic
systems, inducing different persistent organic pollutants (POP) uptake kinetics in comparison with
nutrient-poor systems. The eutrophic system may display lower concentrations of POPs in pelagic
producers. The effect is most obvious during seasons (e.g. spring and summer) or situations in
which plankton have high growth rates.
228 |
in the dissolved state that is subject to volatilisation leads to a decrease in the ow of PCB from
water to the air. The new equilibrium supports the antagonistic process of PCB transport from air
to water. This process is believed to be affected by the abundance of phytoplankton in the water
column (Larsson, 1997).
229
attribute the differences to dilution effects and rather argued that higher growth rates, higher
turnover times and increased sedimentation of pollutants adsorbed to particles lead to the
decreased contamination levels of biota in eutrophic systems.
Taylor et al. (1996) reported high contamination levels of HOCs in large piscivorous sh (especially
salmonids) from the Great Lakes in southern Ontario. Fish in smaller oligotrophic to mesotrophic
lakes had higher HOC concentrations than eutrophic lakes and eutrophic areas within the Great
Lakes. A number of mechanisms were stated to be responsible for changes in nutrient loading
that may change contaminant levels in biota such as: biomass dilution; changes in atmospheric
and/or sediment exchanges; changes in storage lipid content of organisms and changes in food
web structure. It was also revealed that food web structure and lipid content (especially in sh)
have a strong impact on contaminant levels.
Larsson et al. (1998) investigated an oligotrophic and eutrophic lake in southern Sweden that
both received approximately the same atmospheric deposition of PCB. Higher concentrations of
PCB were recorded in the phytoplankton of the oligotrophic lake in comparison with the eutrophic
lake. This was attributed to the higher lipid content found in the phytoplankton community in the
nutrient-poor system. The biota in the oligotrophic system also contained higher amounts of
hydrophobic substances than in the eutrophic system. The concentration of pollutants in plankton
was lower than that found in the sedimenting material indicating that the degradation of lipid
and organic carbon exceeded the release of persistent pollutants from settling particles. Also, no
biomagnication from phytoplankton to zooplankton was detected. Larsson et al. (1998)
concluded that the higher lipid content and higher amounts of pollutant found in the primary
producers suggests a mechanism that lead to high pollutant concentrations in zooplankton and
sh in oligotrophic systems. The major part of the persistent pollutants cycling in the investigated
Swedish lakes was attributed to internal lake processes.
Jeremiason et al. (1999) examined the stresses of trophic condition on airwater exchange and
settling uxes of polychlorinated biphenyls (PCBs) in a paired lake experiment in the Experimental
Lake Area (ELA) in Canada. In the eutrophic lake lower PCB concentrations were detected on
suspended particles, higher PCB settling uxes and lower volatilisation compared to the
oligotrophic lake.
Hylland (1999a,b) carried out a time-trend analysis (1984 1996) of contaminants in cod (Gadus
morhua) in two areas with different eutrophication regimes in the Norwegian Oslofjord. Inputs of
PCBs and trace metals were considered constant between 1981 and 1997. The inner Oslofjord
was characterised by major changes in trophic status over time, while the outer Oslofjord displayed
smaller changes at the same time and was used as a reference site. Cod quality collected from the
outer Oslofjord was reasonably homogenous over time. Cod samples from the inner Oslofjord were
markedly smaller and had lower lipid content from 1984 to 1987 than cod collected between
1988 and 1996. Liver concentrations of the selected PCB, CB 153, differed at both sites between
the years. A similar pattern was observed for the DDT metabolite, DDE. There was no obvious link
between tissue concentrations of the organic compounds and eutrophication status for the inner
Oslofjord. It was concluded that environmental inuences such as oods and not eutrophication
are likely to be responsible for the observed pollutant levels in cod.
230 |
Sderstrm et al. (2000) investigated interactions between eutrophication and organic pollutants:
PCB; DDTs and -HCH in a eutrophic and oligotrophic lake during 1996-1997 in Sweden. The
morphometry, water chemistry and atmospheric exposure of both lakes were similar. The eutrophic
lake displayed higher levels of PCB based on organic carbon and lipid mass in sedimenting matter
in: surface sediment; biota (Perch); higher settling uxes of particulate matter and sediment traps.
No biomass dilution effect was detected. It was suggested that phytoplankton was responsible for
most of the PCB transport to the sediment in the eutrophic lake. Higher DDD/DDE ratios were
related to a high load of p,p-DDT rather than to anaerobic conditions. The oligotrophic lake
showed high DDD/DDE ratio and high sDDT levels in the deep sediment core. The highest ratio
in the sediment traps coincided with the highest runoff of parental DDT from the watershed.
Lithner et al. (2000) studied the direct and indirect effects of eutrophication on turnover of metals
in a paired lake experiment in Sweden. The eutrophic and oligotrophic/mesotrophic lakes were
the same study sites used by Sderstrm et al. (2000; see above). Decreased levels of Pb and Hg
in the eutrophic lake sediments were attributed to signicant dilution effects of pollutants in
seston. The biota (sh) in the nutrient-rich system showed decreased bioavailability of Cd and Tl
but not for Pb and Hg. The observed higher uxes of metals in the eutrophic lake were caused by
the larger biomass and by a different geology and pH. The observed decreased residence time of
Cu, Ni and Tl was attributed to sulphide xation and a reduced concentration of Cd and Mo in
the water column caused by the increased biomass and efcient scavenging of metals.
231
scavenging were resuspension and erosion. It was concluded that it is most likely that eutrophicationinduced scavenging occurred in the Baltic Sea, but natural processes that caused highly variable
burial rates obscured the evidence.
In contrast to the equilibrium partitioning theory (see section 12.3) recent studies (Axelman et al.,
2000; and Larsson et al., 2000) demonstrated that the uptake of organic contaminants is
proportional to the biomass quality. During the gravitational settling of seston from the photic to
the profundal zone, the organic carbon and lipid contents decreased. Larsson et al. (2000)
attributes this decrease to microbial attacks on settling particles. Through this process energy and
nutrients are released and made available for microorganisms. The POP concentration does not
decrease proportionate to the lipid and organic carbon contents during this process but increases
by approximately 10-fold, instead. The POP increase in settling particles varied with environment,
season and concentration. Axelman et al. (2000) point out that traditional equilibrium partitioning
models might underestimate the prediction of HOC concentrations in settling particles and
sediments from concentrations dissolved in the aqueous phase.
The increase of POP concentrations during vertical particle settlement due to microbial attack has
consequences for POP cycling behaviour: the reduction of lipid and carbon traces of particles at
the sediment surface (Axelman et al., 2000; and Larsson et al., 2000); greater incorporation of
POPs into eutrophic, organic/lipid-rich sediments and, consequently, lower pollutant exposure to
pelagic biota in comparison with oligotrophic systems (Larsson et al., 1998; and Larsson et al.,
2000) and high exposure of POPs to profundal benthos foraging on sedimenting matter (Kucklick
and Baker, 1998; and Larsson et al., 2000). Eckhll et al. (2000) and Persson and Jonsson (2000)
investigated laminated sediments in offshore areas in the Baltic Sea and discovered that gross
deposition rates are governed by frequencies of high winds.
Ignatius (1958) rst estimated a mean accumulation rate of approximately 1 mm year-1 over
1000 to 7000 years for the Baltic Sea based on varves in old postglacial Baltic sediments. Jonsson
et al. (1990) used the same technique and estimated accumulation rates in the North-West Baltic
proper of 1.5 4.2 mm year-1 in the unconsolidated upper 5 cm of the sediment during the last
few decades. Jonsson (2000) estimated accumulation rates of 1 - 4.3 mm year-1 for deep areas in
the Baltic Sea based on several studies (Balzer, 1984; Kunzendorf and Christiansen, 1997;
Neumann et al., 1997; Niemist and Voipio, 1974; Niemist and Voipio, 1981; stlund and
Hallberg, 1991; Suess and Erlenkeuser, 1975) that used radionuclids for sediment dating.
Accumulation rates varied with time and between areas (Jonsson, 2000).
Wassmann (1980) investigated the load of POC during lengthy time intervals to the aphotic zone
and the bottom of coastal areas of the boreal North Atlantic using the power model PE = 0.049
PT1.41 (n = 16; r2 = 0.94), where PE is the sedimentation of POC out of the euphotic zone and PT is
the total primary production. The trend in annual PT estimates from the Kattegat was studied for
a time interval of 40 years. Substantial increase of PT was recorded in the southern Kattegat and
interpreted as a consequence of eutrophication. PE increased by about 140 and 250% during that
time period. It was concluded that the increase in POC ux to the aphotic zone was sufcient to
reduce the oxygen concentration in an 8 m deep layer of bottom water to zero. Widespread
occurrences of hypoxia and anoxia in the sediment were attributed to increases in export of
organic matter to the bottom layer caused by eutrophication.
232 |
Resuspension of contaminants
PCB carrying particles normally complete a number of resuspension events before being trapped
in laminated depositional areas of the sediments. The time between the rst deposition of particles
and their associated pollutant to its nal burial can be years to decades. During the transport
particles are subjected to oxic and anoxic degradation that can later lead to slow degradation of
the PCBs once the particle is nally trapped in the laminated sediment (Skei et al., 2000). Strong
energy inputs from waves, currents or submarine slides are mainly responsible for resuspension
events of particle bound PCBs in sediments (Jonsson, 2000). In sediment studies (especially,
retrospective studies) substantial delay mechanisms through resuspension in pollutant-associated
particles have to be considered.
Sulphide oxidation and suspended particulate matter (SPM) uxes in aquatic systems are related
closely to metal resuspension. Lithner et al. (2000) investigated turnover of metals in lakes with
different trophic regimes and found that resuspension and water circulation dominated the ux
of particles at times and biased the overall trend of decreasing Pb loads in sediments due to
decreased atmospheric Pb loads. For substantial improvements of contaminant concentrations
after remedial measures a time lag has to be expected, since sediments can still act as pollutant
sources through resuspension events.
233
deposition of ne material show a highly variable age (days to thousands of years) of carbon (Skei
et al., 2000). Jonsson (2000) stated that Baltic Sea sediments are competent traps of PCB based
on the estimated average retention time of sPCB in the water mass of less than one year. High
sPCB burial rates in the Baltic proper also indicate that laminated sediments are more efcient
traps of PCBs than bioturbated sediment. A comparison between annual burial of PCB in
predominantly laminated sediments of the Baltic proper and bioturbated sediments in the Gulf of
Bothnia indicated that the Baltic had 4 times higher annual burial of PCB.
A large-scale investigation of PCBs in the Baltic Sea sediments was carried out in 1993 in
cooperation of the Baltic States. An increase of sPCBs (IUPAC # 52, 101, 118, 105, 153, 138, 180)
from North to South in surcial sediments was observed indicating atmospheric inuences. Dated
sediment cores from the Baltic proper showed increased or constant concentrations of sPCB during
recent decades, while the pelagic biota contained decreasing PCB concentrations. Down-core
congeners patterns displayed no changes. The calculation of the sediment burial of sPCB suggested
that laminated sediments in the Baltic proper act as efcient traps. A simple mass balance model
indicated that sPCB retention time in the water mass was less than one year (Jonsson, 2000).
Sediments can not be considered as nal sinks for metals due to resuspension (see above,
resuspension of contaminants) events that can reactivate metals bound to sulphides and organic
matter when in contact with oxygenated waters.
234
organic and HOC loads to the sediment may increase as a consequence (Skei et al., 2000). Hoc
concentrations might further increase during vertical settlement of particles associated with
contaminants (see section 12.6) depending on season and environment. These processes may
lead to higher exposure of benthic fauna to HOCs. Experimental studies by Gunnarson et al.
(1996) indicate that the addition of labile organic matter increases the bioaccumulation of
organic contaminants (PAHs) in benthic organisms. These ndings contradict previous assumptions
that enrichment of organic matter in sediments can counteract the bioavailability of HOCs that
might be more rmly attached to organic matter in comparison with minerogenic matter
(Horzempa and DiToro, 1983).
Evers and Smedes (1996) looked at the seasonal variations of PCB and PAH concentrations in
SPM and blue mussels (Mytilus edulis) in the North Sea. Exposure experiments were carried out in
the North Sea at different times of the year (February, July and October) at 16 locations over a
period of 5 years. Additionally, SPM samples were collected quarterly by a continuous-ow
centrifuge. Short-term changes in HOC concentrations were detected in SPM and phytoplankton
that were synchronised within and between different areas. It was suggested that the synchrony
indicated large-scale forces (e.g. certain weather patterns) controlling short-term patterns of HOC
concentrations in suspended matter and various marine organisms. Spatial and temporal trends
in PCB concentration were detected in benthic mussels. Estuarine and coastal locations that
receive contaminants from uvial sources displayed higher PCB concentrations than offshore
locations. Increases of dissolved and particulate organic carbon during periods of high growth
inuenced contaminant concentrations in offshore-SPM and body burdens in mussels. The used
dynamic model predicted the observed SPM accumulation more accurately in comparison with
traditional steady-state models.
Gilek et al. (1996) examined the bioaccumulation and cycling of HOCs in the blue mussel (Mytilus
edulis) from the Baltic Sea at different trophic regimes in a combined laboratory/eld
experimentation and dynamic modelling approach. The rate of HOC uptake was inuenced by
using up to two orders of magnitude by changes in algal food concentrations, while HOC depuration
remained unaffected. It was suggested that trophic-dependent changes were caused primarily by
the inuence of food ration on the physiological activity of the bivalves. Changes in PCB
bioavailability governed by partitioning between water and organic matter (algal food) inuenced
the HOC uptake rate to a lesser degree. For the establishment of a dynamic model, budgets of the
ow of organic carbons and important HOC groups (PAHs, polychlorinated dibenzo-p-dioxins,
furans and PCBs) through the M. edulis community inhabiting the Swedish coastal zone of the
Baltic proper were constructed. The HOC budgets revealed that the bivalve community signicantly
modied the cycling of HOCs in the Baltic proper coastal zone. The net deposition of HOCs to the
bottoms was increased by 13-19%. This increase resulted in a higher availability of HOCs to other
benthic organisms. High bioaccumulation of the contaminants in the tissue of the mussels also
resulted in a higher contamination of demersal sh and waterfowl that feed on M. edulis.
Maloney (1996) investigated interactive processes between organic enrichment and cadmium
(Cd) using 4 benthic species: Amphiura liformis, Amphiura chiajei, Abra alba and Nereis
diversicolor in microcosm experiments over a 10 week period. The partitioning of Cd between the
sediment and pore water phases and bioaccumulation of Cd in the test species were investigated
under different trophic regimes. Sediments and pore water in systems without organic enrichment
235
236 |
deoxygenated conditions. The study showed that the benthic invertebrates accumulated a higher
amount of organic and inorganic contaminants under eutrophic conditions in comparison with the
oligotrophic controls. The bioaccumulation rate of contaminants differed among the selected test
species. Highest contaminant accumulations were found for metals in the bivalve, followed by
metals and benzo[a]pyrene in the polychaete and then benzo[a]pyrene in the brittle star.
Gunnarsson et al. (2000) did laboratory experiments on the effects of inputs of organic matter
(microalgae additions) on bioaccumulation of HOCs (PCBs and PAHs) by the blue mussel (Mytilus
edulis), brittle star (Amphiura liformis) and polychaete (Nereis diversicolcor). Bioaccumulation
appeared proportional to the concentrations of algae and organic carbon. Gunnarsson et al.
(2000) suggested that high nutritional quality of algal organic carbon and feeding rather than
equilibrium partitioning governed the bioaccumulation of HOCs by the benthic test species.
Additionally, eld studies were carried out to measure the annual mass uxes of PCBs in mussels
and brittle stars and contaminant transfer to higher trophic levels. The ndings suggested that
eutrophication processes might contribute to increased HOC accumulation in benthic species. It
was also stressed that temporal variations in quality and quantity of organic carbon have to be
taken into account for assessments of contamination in aquatic systems. Macrofaunal feeding
activities were identied as important for the benthic-pelagic coupling of HOCs. Bioturbation by
the benthic fauna improved the released of HOCs from the sediment to overlying water.
237
Despite their limitations, EUTOX models are an essential tool for risk assessment of aquatic
systems that are impacted by combined pressures of eutrophication and contamination. The
alternation of only single pressures (e.g. reduction of nutrient load) may have fundamental
consequences to the ecosystem (e.g. increased bioavailability of contaminant in water column).
Integrative models can simulate the interactive scenario of eutrophication and contamination
that can support the environmental decision making process.
Continued
Environmental loadings can be from multiple sources such as: constant or dynamic; point or nonpoint sources;
upstream contributions and atmospheric deposition.
1
238 |
zone; removal of an unnecessary conversion from phosphate and nitrate, assuming that all nutrient input is in terms of N and P;
this could affect nutrient limitations; inclusion of an oxygen to organic matter conversion factor (a factor of 1.5) and inclusion of
specic dynamic action in the allometric computation of sh respiration; adding a conversion factor for wind measured at 10 m
height to wind occurring at 10 cm above the water surface in the volatilization computations; for some compounds this could
result in a two-fold reduction in volatilization; nitrication is formulated to occur only at the sediment-water interface and
bioaccumulation, and hence toxicity, are constrained by the life span of an animal.
Assumptions and Limitations:
The aquatic system is assumed well mixed (point model) but stratication can be taken into account.
Model Validation Reports:
The following validation reports are from Release 1 and 1.1. They have not been re-done using the Release 2 code, so the model
results would be somewhat different. But the overall results and conclusions should still be valid.
Download of nutrient analysis on the Onondaga Lake, New York
Download of nutrient analysis of the Coralville Reservoir, Iowa
Download of bioaccumulation of PCBs in Lake Ontario
References:
Koelmans, A.A, A. Van der Heijde, L.M. Knijff and R.H. Aalderink. 2001. Integrated modelling of eutrophication and organic
contaminant fate & effects in aquatic ecosystems. A review. Water Research 15: 3517-3536
Park, R.A., B. Firlie, R. Camacho, K. Sappington, M. Coombs and K.D. Mauriello. 1995. AQUATOX, a general fate and effect
model for aquatic ecosystems. In Proceedings for the Toxic Substances in Water Environments; Assessment and Control, Water
Environment Federation: (3)7-(3)-17
Website:
http://www.epa.gov/waterscience/models/aquatox/
239
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241
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243
BOX 12.6 QUASI Quantitative Water, Air and Sediment Interaction Modied version for EUTOX approach.
Description:
QUASI was originally designed to describe the steady state behaviour of an organic chemical in a lake subject to chemical
inputs by direct discharge, inow in rivers, and deposition from the atmosphere. The mass balance equations for the well-mixed
water column and the well-mixed layer of surcial sediment also include sediment-water exchange by diffusion, deposition, and
re-suspension. Wania (1996) presented a modied version of QUASI to study the interaction of nutrients and contaminants. The
model was parameterised for several typical HOCs in a generic lake and input parameters related to the organic carbon
dynamics were adjusted to reect different trophic conditions.
Most important modications from original QUASI model:
Inclusion of the atmosphere above the lake as a compartment, the concentration of which is calculated rather than being a
model input. This allows for the lake to have an inuence on the concentration in the air above the lake, which may be of
importance for large lakes and chemicals with large air-water exchange uxes. The user has to input the background
concentration in the air owing into the lake area.
Description of the particle-associated transport of HOC on the basis of particulate organic carbon (POC) rather than total
solids, and the derivation of the transport parameters for POC settling, re-suspension and burial within the model.
Calculation of some of the transport parameters describing the atmosphere-water exchange from meteorological and
chemical specic data instead of using generic values.
Programming the model in Stella II-format to facilitate the modelling g of non-steady state scenarios with time-variant input
parameters.
Assumptions and Limitations:
The partitioning of HOCs to DOC or colloidal material is not taken into account.
Application History:
Wania (1996) simulated the interactions between HOCs and nutrients in an eutrophic lake and oligotrophic lake.
Availability and Website:
The original version of QWASI is available at: http://www.trentu.ca/cemc/models/Qwasi.html
References:
Koelmans, A.A, A. Van der Heijde, L.M. Knijff and R.H. Aalderink. 2001. Integrated modelling of eutrophication and organic
contaminant fate & effects in aquatic ecosystems. A review. Water Research 15:3517-3536
Wania, F. 1996. Modelling the Interaction of Eutrophication and hydrophobic organic contaminants behaviour in aquatic
systems. P.R.G. Kramer, D.A. Jonkers and L. van Liere. RIVM report no. 703715001:89-95
244 |
12.9 Summary
Possible interactive mechanisms of HOCs in eutrophic systems are: biomass dilution; growth
dilution, increased sedimentation of contaminant bound pollutants and contaminant burial in
sediments. Consequences for the pelagic biota may be lowered exposure to HOCs in the water
mass and lower bioaccumulation of contaminants. In extreme cases, eutrophication alone may
lead to anoxic conditions in the bottom sediment and the benthic fauna becomes extinct.
Increased sedimentation rates and the effect of increased POP concentrations during vertical
settlement of particles due to microbial attacks may increase exposure of benthic fauna foraging
on sedimenting matter. Pollutants may be increasingly bioaccumulated in the benthic organisms
and contamination of predatory animals feeding on benthic invertebrates (e.g. demersal sh and
waterfowl feeding on bivalves) can occur.
In oligotrophic systems smaller biomass in the water column may result in higher concentrations
of HOCs in the dissolved aqueous phase in comparison with nutrient-rich systems. Pelagic biota
may bioaccumulate higher amounts of pollutants. Sedimentation of particle bound HOCs is
decreased compared with eutrophic systems and benthic fauna less exposed to pollutants in
sediments.
The case studies presented in this report conrmed that the pelagic biota accumulated lower
amounts of organic contaminants in eutrophic systems. The important interactive mechanisms
identied were: biodilution, changes in storage lipid content of organisms, and changes in food
web structure. Higher lipid contents and higher amounts of pollutants in primary producers can
lead to mechanisms that result in higher pollutant concentrations in the biota of oligotrophic
systems. However, some episodic events, such as oods can override interactive processes and no
obvious link between pollutant levels in the pelagic biota and eutrophication may be found.
Most case studies relating to the benthos investigated the impact of organic enrichment on
bioaccumulation of pollutants in benthic biota. Benthic invertebrates accumulate higher amounts
of organic and inorganic contaminants under eutrophic conditions. Bioaccumulation was found
to be proportional to concentrations of algae and organic carbon and high nutritional quality of
algal organic carbon and feeding were responsible for bioaccumulation of HOCs. Further, HOC
uptake was dependent on food concentrations, and trophic-dependent changes were caused by
physiological activities of bivalves inuenced by food rations.
Internal factors in aquatic systems can inuence interactive mechanisms between eutrophication
and contamination. The composition of lipids in aquatic organisms, for example, is crucial for the
fate of hydrophobic contaminants. The equilibrium partitioning between contaminants in the
water column and biomass in aquatic systems needs to be quantied for different scenarios since
it is decisive for the biodilution effect.
The single pressures of eutrophication and contamination may both induce changes in the aquatic
system. Effects of eutrophication may be: increased productivity; increased sedimentation after a
bloom; organic enrichment of sediments resulting in hypoxia or anoxia. These and other alterations
(e.g. reduced light conditions) related to eutrophication can inuence the species composition
and diversity structure of phytoplankton, zooplankton, pelagic and benthic communities (Skei et
al., 2000).
245
Contaminants can cause direct toxic effects when released in certain concentrations into the
aquatic environment. Toxicant induced lethality can decimate sensitive species and/or sublethal
effects may change physiological activities (e.g. reproduction, growth, maturation, longevity) of
the biota. These ecological alterations can lead to a trophic cascade or release from competition
inuencing secondarily tolerant species (Fleeger et al., 2003). The extent of the direct and/or
indirect effects of contaminant exposure on biota is concentration dependent and environmental
quality standards (EQS) regulate the amounts of discharge of selected priority substances.
Interactive effects of chemical mixtures occurring in aquatic systems and their additive, synergistic
and antagonistic effects on biota have not been investigated adequately and relationships have
not yet been quantied.
Additionally to knowledge based on quantied impacts of the single pressures eutrophication/
contamination and risk assessment using ecological models (e.g. ECOPATH), pollutant interaction
has to be considered for environmental decisions and water management. A reduction of nutrients,
for example, improving the trophic status may also lead to an increase of contaminant concentrations
in the system and higher bioaccumulation of toxicants in the pelagic biota. Additionally, improved
oxygen conditions at the bottom may lead to recolonisation of laminated sediments by benthic
fauna. As a result of bioturbation and geochemical processes, contaminants that were previously
trapped in the sediments may be mobilised. The level of contaminants may, vice versa, inuence
the primary production and indirectly the status of eutrophication (Skei et al., 2000).
Interactions between eutrophication and contaminants have to be investigated further to predict
their effects under changing environmental conditions. There has been some work done on
interactions between hydrophobic organic compounds and trophic status (Skei et al., 2000) but
more knowledge is needed on interactive processes between metals and other toxic substances
and eutrophication. Relationships should be quantied to support water management and
remedial measures.
Ecological models from the category of the new EUTOX models (e.g. AQUATOX) are capable of
simulating chemical fate/effect and food chain accumulation at varying trophic levels. The
restricting factor of the new models types are that long term simulations of exposure, food chain
bioaccumulation and toxicity remain uncertain on the ecosystem level due to the superimposition
of chemical fate model descriptions on ecological model constructs (Koelmans et al., 2001).
Despite their limitation, EUTOX models are useful tools for risk assessment of habitats under
combined pressures of nutrients and contaminants.
The identied interactive mechanisms between eutrophication and contaminants raise further
questions about their importance in the aquatic system. The following ten questions reect
knowledge gaps that future research need to answer to enable water policy makers to consider
combined effects of eutrophication and contaminants in water management.
1. What are the consequences for aquatic systems under pressure from both eutrophication
and contamination if only one pressure is altered?
2. To what extent will the concentrations of contaminants in the water mass and pelagic biota
increase if the nutrient input is reduced without simultaneous reduction of contaminant
inputs?
246 |
3. Under what circumstances do sediments act as sinks or sources for contaminants in systems
with different trophic regimes?
4. To what extent will decreased eutrophication inuence the bioavailability of contaminants?
5. Can the relationships between the combined pressures of eutrophication and contamination
and the pelagic and benthic biota be quantied?
6. Can key species be identied that indicate the interactive effect of eutrophication and
contamination?
7. Under what circumstances do the effects of biodilution and growth dilution override other
internal factors in eutrophic systems and lead to lowered exposure of the pelagic biota to
contaminants?
8. To what extent will a reduced sedimentation of organic matter inuence the concentrations
of contaminants in the benthic biota?
9. To what extent does the benthic biota reintroduce contaminants into the pelagic biota
through the food chain in eutrophic systems that show lowered contaminant concentrations
in the water mass and higher concentrations of contaminants in the sediments?
10. To what extent does remobilisation of contaminants by bioturbation of re-colonised
laminated sediments after improvement of oxic conditions occur?
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Fleeger, J.W., K.R. Carman, and R.M. Nisbet. 2003. Indirect effects of contaminants in aquatic ecosystems.
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Maloney, J. 1996. Inuence of organic enrichment on the partitioning and bioavailability of cadmium in a
microcosm study. Marine Ecology Progress Series 144:147-161
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European Commission
EUR 22314EN DG Joint Research Centre, Institute for Environment and Sustainability
Editors: Angelo G. Solimini, Ana Cristina Cardoso and Anna-Stiina Heiskanen
Luxembourg: Office for Official Publications of the European Communities
2006 VIII, 252 pp. 17 x 24 cm
Scientific and Technical Research series
ISSN 1018-5593
ISBN 92-79-02646-1
The Water Framework Directive (WFD) defines the ecological status of surface waters as an expression of the quality of the structure and functioning of aquatic ecosystems. This book provides an
overview of current knowledge on the relationships between anthropogenic pressures and biological indicators for rivers, lakes and coastal waters. It is targeted at scientists working in environmental agencies, managers working on WFD implementation, university lecturers, students of applied
ecology, water management and those interested in limnology and coastal management.
Each section is dedicated to one of the major pressure types: eutrophication and organic pollution,
acidification, hydromorphological, toxic, and combined pressures which are currently most widely
impacting surface waters in Europe. In each chapter we aim to provide a concise and factual overview on the known relationships between the pressure type in question and the biological responses, for different surface water categories (rivers, lakes, coastal and transitional waters). We have
compiled information on the applicability of the current existing biological classification tools and
metrics, as well as the empirical and deterministic models which include biological quality elements
as parameters, and could be used for WFD classification and management purposes. Finally, we
also provide information on some new emerging approaches and methodologies that could be applied in the future.
This book is a deliverable of the EU FP6 REBECCA (Relationships between ecological and chemical
status of surface waters) project. The general objective of the REBECCA project is to provide scientific support for the implementation of the WFD. The two specific aims of the project are, firstly, to
establish links between ecological status of surface waters and physico-chemical quality elements
and pressures from different sources, and, secondly, to develop and validate tools that member
states can use in the process of classification, in the design of their monitoring programs, and in
the design of measures in accordance with the requirements of the WFD.