Environment International 37 (2011) 778–801

Contents lists available at ScienceDirect

Environment International
j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / e n v i n t

Review

Coastal marine eutrophication assessment: A review on data analysis

Dimitra Kitsiou ⁎, Michael Karydis
Department of Marine Sciences, School of the Environment, University of the Aegean, Mytilini, GR-81100, Greece

a r t i c l e i n f o a b s t r a c t

Article history: A wide variety of data analysis techniques have been applied for quantitative assessment of coastal marine
Received 5 July 2010 eutrophication. Indicators for assessing eutrophication and frequency distributions have been used to develop
Accepted 7 February 2011 scales for characterizing oligotrophy and eutrophication. Numerical classification has also contributed to the
assessment of eutrophic trends by grouping sampling sites of similar trophic conditions. Applications of
Keywords:
eutrophication assessment based on Principal Component Analysis and Multidimensional Scaling have also
Statistical methodology
Multicriteria analysis
been carried out. In addition, the rapid development of Geographical Information Systems has provided the
Spatial analysis framework for applications of spatial methods and mapping techniques on eutrophication studies. Satellite
Geostatistics data have also contributed to eutrophication assessment especially at large scale. Multiple criteria analysis
Mapping methods can integrate eutrophication variables together with socio-economic parameters providing a holistic
GIS applications approach particularly useful to policy makers. As the current concept of eutrophication problems is to be
examined as part of a coastal management approach, more complex quantitative procedures are needed to
provide a platform useful for implementation of environmental policy. The present work reviews methods of
data analysis used for the assessment of coastal marine eutrophication. The difficulties in applying these
methods on data collected from the marine environment are discussed as well as the future perspectives of
spatial and multiple criteria choice methods.
© 2011 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 779
2. Definitions of eutrophication . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 780
3. Ecosystem variables used in eutrophication assessment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 781
4. Shortcomings in data analysis for assessing eutrophication . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 782
5. Indicators for assessing eutrophication . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 782
6. One-dimensional statistical analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 783
6.1. Descriptive statistics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 783
6.2. Frequency distributions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 784
6.3. Outliers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 784
6.4. Analysis of variance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 785
6.5. Correlation and regression . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 785
7. Multi-dimensional statistical analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 786
7.1. Principal Component Analysis (PCA) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 786
7.2. Cluster Analysis (CA). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 786
7.3. Discriminant Analysis (DA) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 788
7.4. Multidimensional Scaling (MDS) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 788
7.5. Correspondence Analysis (COA). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 788
7.6. Gradient Analysis (GA) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 788
8. Multiple Criteria Analysis (MCA) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 788
9. Remote sensing. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 790
10. Spatial analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 790
11. Mapping . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 791

⁎ Corresponding author. Tel.: + 30 22510 36819; fax: + 30 22510 36809.

E-mail address: dkit@aegean.gr (D. Kitsiou).

0160-4120/$ – see front matter © 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.envint.2011.02.004
 D. Kitsiou, M. Karydis / Environment International 37 (2011) 778–801 779

12. Modeling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 791

13. The need for an integrated approach . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 792
14. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 795
Acknowledgment. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 797
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 797

1. Introduction marine environment from local sources include agriculture, energy

Eutrophication is a natural process characterizing excessive algal
growth due to nutrient supply to the marine systems. Physical factors
such as the geomorphology of the system, the mean depth of the
area and the prevailing currents are the main factors affecting the
process (de Jonge et al., 2002). The terms “eutrophic”, “mesotrophic”
and “oligotrophic” were proposed as early as 1907 to describe plant
growth induced by nutrient supply to German swamps (Weber,
1907). These terms were introduced into limnology by Naumann
(1919) providing a classification scheme according to plant produc-
tion and nutrient availability (Hutchinson, 1967). A classification
trophic scheme was proposed by Naumann in 1929 for lake water types
based on production of organic matter by phytoplankton as well as
primary physical and chemical determinants (Wetzel, 2001). According
to this scheme, lake water type was characterized as oligotrophic,
eutrophic, acidotrophic, alkalotrophic, argilotrophic, sidetrophic and
dystrophic. Later, this scheme was modified and water types were
classified as ultraoligotrophic, oligotrophic, mesotrophic, eutrophic
and hypertrophic (OECD, 1982) on the basis of phosphorus loading
and of algal densities. This five class scheme was also adopted for the
marine environment (Nixon, 1995). Coastal marine eutrophication was
recognized as a problem of “disturbance” of the marine ecosystems
since the 60s (Postma, 1966; van Beusekom, 2005). Due to the
complexity of causes, effects and processes concerning eutrophication,
a number of definitions have been proposed by both researchers and
international organizations (Vollenweider, 1992; Gray, 1992; Heip,
1995; Nixon, 1995; UNEP, 1999; EEA., 1999).
In addition to the complex processes in coastal waters and the
human impacts that make the assessment of eutrophication difficult
(Andersen et al., 2006a), the boundaries of the coastal waters cannot be
easily defined. Coastal waters include estuaries, gulfs and coastal seas
that can extend to the continental shelf which means they cover an area
shallower than 200 m (Crossland et al., 2005). However, hydrodynamic
and ecological conditions in the coastal marine zone are greatly
influenced by a number of abiotic factors: geometry of the coastline,
bathymetry of the area, wave action, mixing characteristics and the
retention time differentiate coastal water masses from offshore waters.
In addition, physical factors such as light penetration and advective
forces (Painting et al., 2005) moderate unwanted effects and influence
the ecosystem sensitivity of different water masses to nutrient
enrichments. This is why there is no single definition of the coastal
zone. There are various definitions referring to spatial boundaries
ranging from very broad areas such as coastal seas to very restricted
coastal areas that are under the immediate influence of human actions.
It is therefore advisable that the boundaries of coastal waters should not
be always defined a priori but after consideration of the features
mentioned above. In addition, the definition of the coastal zone should
vary according to the type of the problem addressed and the objectives
set to study the particular problem (Harvey and Caton, 2003).
The coastal zone is also a complex system from the ecological point of
view: many unique ecosystems are adapted to high nutrient flows from
terrestrial sources and sediment resuspension, high biological produc-
tivity and high diversity (Crossland et al., 2005). Coastal marine
ecosystems undergo through continuous changes in rates of production,
species abundance and community structure. These changes reflect the
impact of global effects such as climatic changes as well as the impact
from local and regional effects (Tyson et al., 2001). Pressures on the
production, industrial activities, transport, tourism, fishing and fish
farming. It is difficult for all those activities to become environmentally
friendly since they have been designed in a macroeconomic context and
some of them a long time ago (Crossland et al., 2005).
Nutrient fluxes into the marine environment may be due to point
sources such as sewage effluents (treated or untreated) and discharges
from industrial plants as well as from non point sources mainly
run off from agricultural catchments. Nutrient loads cause a variety of
impacts: high levels of chlα, excessive growth of seaweeds, algal
blooms sometimes toxic, reduction in abundance/biodiversity and
decreased water transparency; in more advanced stages high bacteria
levels, scums, fungi, hypoxia and finally anoxia is observed. Potential
consequences of eutrophication to humans may range from nuisances
such as allergies and dermatitis to serious health threats (Ferreira
et al., 2007). Eutrophication is considered as a type of regime shift.
In particular, eutrophication of freshwater lakes and reservoirs is a
well-known type of regime shift caused by the excessive fertilization
of aquatic ecosystems by phosphorus (Carpenter, 2003). Regime
shifts are abrupt changes between contrasting, persistent states of a
system and are thought to be driven by external perturbations or by
the system's internal dynamics; however, the exact mechanism is
often unclear (deYoung et al., 2008). Schramm (1999) recognized
light and temperature as key abiotic factors controlling algal growth,
although nutrient loading is one of the most important drivers of
regime shifts in transitional waters.
Ecological research on eutrophication has provided vast amounts
of data and adequate understanding of biogeochemical processes
related to the problem of eutrophication. A lot of research has also
been carried out to quantify eutrophic trends (Nixon, 1995; Ferreira
et al., 2007). However, there are shortcomings related to methods
used for data analysis. In addition there is a doubt about the ecological
effectiveness of qualitative measures “to provide a basis for practical
action in environmental problems” (de Jong, 2006). Policy makers
claim that the research findings cannot be easily incorporated in the
legislation or implemented in management strategies. On the other
hand, researchers are reluctant to condense the information to a
binary system “good” or “bad” water or even in an ordinal scaling
because of loss of significant information. Numerous data processing
techniques have been proposed that can be used for eutrophication
assessment (Digby and Kempton, 1987; Krebs, 1999; de Jonge et al.,
2002; Zuur et al., 2007).
Assessment of eutrophication requires data collection. These data
can be collected either within the framework of a monitoring program
(UNEP, 2003) or as targeted projects. Data collection techniques depend
on the variable to be measured and project objectives (Bierman et al.,
2011). Field work can be carried out either by in situ sampling, using
moored instruments as well as by ship opportunity measurements.
These data can form the basis for a number of data processing techniques
that summarize the information and show possible eutrophic trends in
the marine environment (Danilov and Ekelund, 2001).
Ecological indicators (Karydis, 2009) are among the most popular
methods for condensing ecological information. However, there is loss
of qualitative information (taxa) and possibly loss at quantitative level
regarding the spatial and temporal dimensions of the ecosystem
variables. Many ecological indicators have also formed the basis of a
scoring system to characterize trophic status (Spatharis and Tsirtsis,
2010), especially for the implementation of the Water Framework
780 D. Kitsiou, M. Karydis / Environment International 37 (2011) 778–801
Directive (EC., 2000; Borja and Dauer, 2008). This is a five level water
quality classification scheme (High, Good, Moderate, Poor and Bad).
According to the European Directive phytoplankton parameters are
fundamental in assessing trophic states; chlα concentration, species
abundance, species composition and frequency of algal blooms. The
data can be historical, from current field sampling or even simulated
data (Primpas and Karydis, 2010a). Historical data can form a basis
for comparisons and can provide information on temporal trends
especially if the field information has been based on monitoring
projects. Simulated data derived from either statistical or dynamical
modeling are clear of noise but their reliability must be under
question every time they are used for a specific application. It is
therefore important that assessments should be based on different
methodological approaches leading to a convergence in water quality
or ecosystem quality (Moriki and Karydis, 1994; Karydis, 1996).
There are many multivariate techniques (Sharma, 1996) that have
been used to analyze spatial trends (Karydis, 1992; Ignatiades, 2002b)
or just to eliminate the number of variables (Zitko, 1994) in ecological
studies. These data analysis processes use discrete samples; the
ecosystem descriptors can be chemical variables (nutrients), physical
variables (temperature, salinity and transparency), biological vari-
ables (chlα, phytoplankton cell number and ecological indices) or
phytoplankton community structure. The multivariate techniques
widely used in marine pollution studies and evaluation of environ-
mental data are Principal Component Analysis (Zitko, 1994), Cluster
Analysis (Clarke, 1993), Multivariate Dimensional Scaling (Warwick
et al., 1988), Discriminant Analysis (Aguilera et al., 2001) and Factor
Analysis (Ignatiades et al., 1992). The main shortcoming of these
methods is lack of a statistical evaluation of the obtained results; the
exceptions are rather rare (Vassiliou et al., 1989).
During the last decades, the rapid development of Geographical
Information Systems (GIS), established them as an indispensable tool
for supporting decision-making in coastal areas, with significant
contribution to the development of Integrated Coastal Zone Manage-
ment (ICZM) tools (Kitsiou et al., 2002). Coastal marine eutrophica-
tion assessment, an important component of ICZM approaches has
been further supported by the application of a variety of spatial
analysis methods, geostatistical analysis and mapping techniques,
frequently performed in the framework of GIS. The development of
accurate spatial databases in a GIS environment and the production of
maps illustrating the eutrophication trends of coastal areas in a clear
and simplified way constitute an important improvement in eutro-
phication studies (Xu et al., 2001). In addition, the development of
remote sensing techniques and the processing of satellite data offered
new directions in eutrophication studies, since data sets at large
spatial scales can be available at low cost. Furthermore, a wide range
of modeling approaches ranging from one to multi dimensional,
have been developed and applied to assess the interrelations among
the various parameters related to eutrophication and to predict the
response of coastal ecosystems to forcing from both physical and
anthropogenic activities (Tett et al., 2003). Multiple criteria analysis
methods have been widely applied in the field of economics and
policy analysis (Janssen, 1992) and during the last decade, for
assessing environmental issues. They have been proved very useful
in assessing eutrophication trends in coastal areas; therefore they are
frequently included in methodologies related to coastal management
and decision-making. Their characteristics have established them as
an important tool in policy analysis, physical planning (Pettit and
Pullar, 1999), environmental and coastal management (Linkov et al.,
2006; Ananda and Herath, 2009) and environmental decision-making
(Hajkowicz, 2007).
The review is structured into the following parts: Background
information (Sections 2–4), Indicators (Section 5), Statistical methods
(Sections 6–7), Multiple criteria analysis (Section 8), Spatial methods
(Sections 9–11), Modeling (Section 12) and Integrated approaches
(Section 13). The first part reviews definitions of eutrophication and
examines the variables used in eutrophication studies. Indicators
are evaluated according to their effectiveness for assessing eutrophi-
cation effects. Statistical methods for quantifying trophic status are
presented and their potentiality/shortcomings are discussed. Multiple
criteria methods have also been considered as powerful tool for
assessing eutrophication as they can combine eutrophic effects with
social and economic aspects of the coastal zone; they can also examine
different scenarios of coastal management and development. Spatial
methods widely used in eutrophication studies (remote sensing,
spatial analysis and mapping techniques) are presented and their
advantages/shortcomings to assess the trophic status in marine coastal
areas at different spatial scales are discussed. A short description of
modeling approaches to describe eutrophication dynamics is also
included. The interaction of the different data analysis methods and
methods integrating information from different scientific disciplines
for assessing coastal eutrophication are presented; their importance
in designing nutrient management strategies to mitigate eutrophic
impacts is also discussed.
2. Definitions of eutrophication
Naumann was the first to define lake eutrophication in 1919 as the
increase of nutritive substances in a lake, especially phosphorus and
nitrogen (Hutchinson, 1967). Later, the term eutrophication was
interpreted in a broader sense: it included “any and all nutritive
substances” (Halser, 1947). However, all these definitions were
developed for lake waters. As the understanding of eutrophic
processes in the marine environment was improving, eutrophication
was redefined. According to Steele (1974), “Eutrophication is the
increase of the growth rate of algae, following a faster rate of nutrients
in the marine environment as well as the consequences”. Vollenweider
(1992) has given a more comprehensive definition on eutrophication
referring in more detail to the impacts: “Eutrophication — in its more
generic definition that implies to both fresh and marine waters — is the
process of enrichment of waters with plant nutrients, primarily
nitrogen and phosphorus that stimulates aquatic primary production
and its more serious manifestations lead to visible algal blooms, algal
scums, enhanced benthic algal growth of submerged and floating
macrophytes”. A definition was also given by Gray (1992), exempting
the impact of toxic compounds entering the ecosystem: Eutrophica-
tion occurs “when nutrients are added to the body of water they load,
provided they are not toxic compounds and provided that there is
sufficient light to increased autotroph growth and also to increased
heterotroph growth”. A very short and simple definition has been
given by Nixon (1995). “Eutrophication is an increase in the rate of
supply of organic matter to an ecosystem”. This definition does not mix
causes effects relationships and is limited to the main process which is
the biomass production and places emphasis on eutrophication as a
process. Since this definition refers to the increase of the supply of
organic matter, it links the responses of coastal water masses to
organic industrial and urban effluents. Similar views seem to be shared
by Heip (1995) as “nutrient increase leads to a number of problems
when benthos is considered”: the impact from nutrient loading is not
always having a direct effect on primary production as nutrients may
be transferred from a distance either as part of living biomass or as part
of dead organic matter. In addition to increased primary production,
indirect effects may be observed such as oxygen depletion, changes in
species composition and species interaction. Nixon's definition does
not take into account nitrogen and phosphorus that is the limiting
nutrients that can be recycled several times contributing to carbon
fixation. Another point of critics is the fact that monitoring of primary
production is rather expensive (Nixon, 2009) and therefore data
collection will be limited.
A number of definitions have also been given by international
bodies focusing on practical aspects. The European Environmental
Agency in a report on eutrophication in Europe's coastal waters (EEA,
 D. Kitsiou, M. Karydis / Environment International 37 (2011) 778–801
2001), although they accept Nixon's definition, for practical reasons
they state that “in this report eutrophication means enhanced primary
production due to excess supply of nutrients from human activities,
independent of the natural productivity level for the area in question”.
However, in the European Union Directive on urban waste water
treatment, the emphasis is placed on nitrogen and phosphorus
enrichments that is the two nutrients that have to be removed
during the sewage treatment: “The enrichment of water by nutrients,
especially compounds of nitrogen and/or phosphorus, causing an
accelerated growth of algae and higher forms of plant life to produce
an undesirable disturbance to the water balance of organisms present
in water and to the quality of the water concerned” (EC, 1991a); this
definition has also been proposed by a working group on “Eutrophi-
cation in European Ecosystems” (EEA, 1999). UNEP (2003) emphasizes
on the production of organic matter: “Eutrophication is defined as an
environmental disturbance caused by excessive supply of organic
matter”. The definitions mentioned above have a point in common:
they all consider eutrophication as a “disturbance” that is a reversible
change in the ecosystem and not as a form of pollution characterized
by environmental degradation. In 2001, Cloern identified three phases
in the studies on eutrophication. The Phase I model was strongly
influenced by the conceptual models of eutrophication developed by
limnologists. In this approach, the rate of nutrient loading sets the
rates of phytoplankton population growth and biomass accumulation.
In the Phase II model the response to nutrient enrichment includes
changes in the biomass of algal communities such as macroalgal and
microphytobenthos, shifts in phytoplankton community composition
and harmful algal blooms. These direct responses can lead to a suite of
indirect responses such as changes in water transparency, distribution
and abundance of vascular plants, mortality of fish/invertebrates,
inputs of organic carbon to sediments with another suite of changes
in the biogeochemistry of the sediments. The Phase III model has a
broader perspective and considers the social, economic and human
health costs of coastal eutrophication and the impacts of nutrient
loading on the Earth System. Therefore, a set of tools should be
produced to support rational management strategies and action plans
for ecosystem rehabilitation/restoration (Cloern, 2001).
Among the two schools of thought on the definition of eutrophica-
tion i.e. the causal relation between nutrient (N, P) — plant biomass
production and the production of organic matter, the first approach
seems to be more reasonable. Historically eutrophication was estab-
lished as increased plant production stimulated by inorganic N and
P compounds. Furthermore these limiting nutrients seem to control
carbon fixation and therefore production of plant biomass. This form
of definition has been accepted not only on a scientific basis (Steele,
1974; Gray, 1992; Vollenweider, 1992; O'Sullivan, 1995; Smith et al.,
1999; de Jonge et al., 2002) but also in a number of legal documents (EC,
1991b; MAP, 2008; UNEP, 2009). It combines the scientific background
of eutrophication with practical aspects of eutrophication mitigation
and management.
3. Ecosystem variables used in eutrophication assessment
The phenomenon of eutrophication has been recognized as a
problem worldwide over the last decades (Vollenweider, 1981).
Nutrients, phytoplankton biomass and organic matter mentioned in
the definition section form the “keywords” indicating the variables that
primarily should be monitored. The major nutrients causing eutrophi-
cation are nitrogen and phosphorus. In lake waters phosphorus is
usually due to inputs from terrestrial sources of phosphorus. However,
early studies in nutrient limitation and eutrophication in coastal marine
waters (Dugdale, 1967) have clearly shown that nitrogen is the limiting
nutrient in coastal systems (National Academy of Sciences, 2003).
However, in some areas like the Eastern Mediterranean System (EMS)
it has been observed (Krom et al., 1991) that EMS was phosphorus
limited. The nitrogen to phosphorus ratio was found unusually high
781
(28:1) and as a consequence the winter phytoplankton bloom was
phosphorus rather than nitrogen limited (Krom et al., 2010). The
phosphorus limited character of EMS was also confirmed by Thingstad
and Rassoulzadegan (1995).
It is obvious that for monitoring eutrophication in the marine
environment a large number of variables beyond nitrogen and
phosphorus are needed. This is necessary as monitoring in policy
making can trigger enforcement action whereas, in research can
contribute to the understanding of interrelationships between variables
and the ecological processes triggered by marine eutrophication.
Measurements on nutrients from riverine inputs are crucial in assessing
the enrichment of the marine environment in nitrogen and phosphorus.
OSPAR recommends data collection on inputs, nitrate of total nitrogen,
phosphate and total phosphorus in the NE Atlantic on a systematic basis
(OSPAR/ASMO, 1998). HELCOM (1998) recommends data collection on
total nitrogen and total phosphorus in the Baltic Sea. MED POL
recommends to the member states monitoring of nitrate, ammonium
and phosphate in the Mediterranean from major rivers (EEA, 1999). The
same variables are recommended for monitoring in areas near sewage
discharges from the main coastal cities of the Mediterranean. IFREMER
has proposed a number of physical, chemical and biological variables
for assessing eutrophication in lagoon ecosystems (Zaldívar et al.,
2008a). Dissolved oxygen, turbidity, nitrite, nitrate, ammonia, chlα,
total nitrogen and total phosphorus are the variables proposed for the
water column; whereas organic matter, total nitrogen and total
phosphorus are recommended for the sediment, species richness and
population densities have been proposed for macrobenthos and species
biomass as well as diversity for macrophytes.
Within the framework of the MED POL ongoing Mediterranean
monitoring program (UNEP, 2003) a decision was made concerning the
mandatory parameters that should be monitored by each Mediterra-
nean State Member. These are temperature, pH, transparency, salinity
(psu), orthophosphate (P–PO4, μg-at/l), total phosphorus (P, μg-at/l),
silicate (SiO2, μg-at/l), dissolved oxygen (mg/l), chlα (μg/l), total
nitrogen (N, μg-at/l), nitrate (NO3–N, μg-at/l), ammonium (NH4–N,
μg-at/l), nitrite (NO2–N, μg-at/l) and phytoplankton (cell number and
species composition). All these proposed variables as well as the
suggestion for collecting and using historical records, aim at specific
objectives: (a) in areas sensitive to eutrophication phenomena such as
coastal bays, lagoons and estuaries to be able to discriminate between
natural fluctuations in nutrient and phytoplankton concentrations from
anthropogenic pressures (b) to assess the progress in the quality of the
marine environment after the adoption of the European Union
Directives, directly or indirectly related to the problem of eutrophica-
tion, such as the nitrates directive and the water quality directive as well
as other national legislations and international conventions and (c) this
information combined with drivers, pressures, meteorological and
hydrodynamic parameters can provide a better understanding of the
problem of eutrophication and contribute to coastal management
practices and scenarios for coastal development.
The tendency in eutrophication studies is to increase the number
of variables used for quantitative assessment of eutrophication.
Although a wide array of physical, chemical and biological variables
contributes to the understanding of coastal marine eutrophication
processes, it is doubtful whether they are all necessary in assessment
studies. Taking into account the definition of eutrophication linking
nutrient availability to plant biomass production, the number of
variables needed for eutrophication assessment is rather limited:
inorganic nitrogen (nitrate, nitrite and ammonia), inorganic phos-
phorus (orthophosphates) and production of organic matter (chlα,
phytoplankton cell number and macrophyte biomass) seem to be
adequate in eutrophication assessment. There are several advantages:
(a) inexpensive monitoring (b) large existing data bases of historic
data (c) combination of pigment measurements with satellite
imagery to provide a description of marine eutrophication at a spatial
scale and (d) most of the methods described in the present work can
782 D. Kitsiou, M. Karydis / Environment International 37 (2011) 778–801
be applied using the above mentioned variables. These variables are
considered adequate in marine monitoring; however, information on
community structure can also provide useful information on
quantifying eutrophication trends. This approach can contribute to
the understanding of the role of species and species diversity in
ecosystem functioning under conditions of nutrient enrichment. It can
therefore be useful at a limited extent.
4. Shortcomings in data analysis for assessing eutrophication
In spite of the easiness in laboratory determination of nutrients,
chlα concentrations, phytoplankton biomass and phytoplankton
community analysis, data processing seems to face a number of
problems. (a) The nutrient variables, nitrate, nitrite, ammonia and
phosphorus, chlorophylls, phytoplankton cell number, ecological
indices and water transparency that are the main parameters
characterizing trophic states are highly intercorrelated (Ignatiades
et al., 1985; Primpas et al., 2010). This means that the total effect
expressed through these variables is not additive and in some cases
uncorrelated variables must be obtained (Primpas et al., 2010). (b)
The frequency distributions of the above mentioned variables do not
follow normality. An analysis of 950 samples collected from 25 meso
and hypertrophic lakes in Sweden (Heyman et al., 1984) has shown
that nutrient variables were log normal whereas chlα values best
fitted to the gamma distribution. Similar results for nutrient variables
were found in sets of data collected from the Aegean (Ignatiades et al.,
1992) but chlα values seemed to fit log normality (Primpas and
Karydis, 2010a). These distributions assume data transformations
to normalize the variables when parametric methods are applied.
However, transformations tend to compress the values so a great deal
of the information of the raw data is lost. (c) Seasonal trends in
nutrient concentrations (Pagou and Ignatiades, 1988) and phyto-
plankton cell number (Ignatiades et al., 1986) show increased
variations around mean values, resulting into overlapping among
sets of data characterizing oligotrophic, mesotrophic and eutrophic
conditions (Giovanardi and Tromellini, 1992). (d) Discrimination
between natural and anthropogenic causes of marine eutrophication:
as nutrients and phytoplankton are built-in variables in the aquatic
ecosystems, it is difficult to know which loads come from human
activities. Use of control or reference sites is not always a solution to
the problem since offshore sampling sites may represent a different
type of ecosystem than the shallow coastal marine environment.
Nutrient concentrations causing eutrophication depend on the
topography, the physical and the chemical nature of each coastal
area. ‘Excessive’ nutrient concentrations should be compared to the
‘background’ or ‘reference’ values for a particular area. Reference
values are different in different seas such as the oligotrophic
Mediterranean and the eutrophic North Sea (EEA, 1999). However,
reference levels are not easy to establish due to nutrient dynamics
and human impacts.
5. Indicators for assessing eutrophication
The term “indicator” is often used in the marine environment to
describe ecological status, to assess water quality and to provide
practical information for coastal management practices. As the
concept of an indicator in ecology is different from the concept of
an indicator in applied fields such as pollution, management and
planning, it becomes obvious that no single definition of indicator
can satisfy this wide spectrum of uses and applications. According to
a simple definition (Walz, 2000), “An indicator is a variable that
describes the state of the system”. An indicator definition oriented to
ecological and water quality status has been given by Ferris and
Humphrey (1999): “An indicator may be defined as a characteristic
which, when measured repeatedly, demonstrates ecological trends
and a measure of current state or quality of an area”. Ferris and
Humphrey had in mind the use of biodiversity indicators for assessing
environmental quality. A definition of an indicator in a broader sense
has been given by Burger (2006): “Indicator: Index or measurement
end point to evaluate health of a system; physical, biological,
economic and human”. Popular ecological indices (i.e. Shannon's
index) should be used with care in eutrophication studies as a number
of problems arise: (a) It is difficult to define empirically reference
conditions (Nielsen et al., 2007). (b) Although richness and diversity
are well established variables, describing the ecological state of
an ecosystem, their values can be erroneous as far as the assessment
of eutrophication is concerned: phytoplanktonic invasive species
increase the diversity values although this high diversity values
does not mean better water quality. If the invasive species are toxic
then the deficit of the index is even stronger. (c) Indices used for
eutrophication assessment should show monotonicity, in other words
they should consistently increase or decrease along the eutrophica-
tion gradient.
Statistical multivariate methods have been applied to evaluate
popular ecological indices in marine eutrophication assessment
studies in coastal areas (Karydis and Tsirtsis, 1996; Danilov and
Ekelund, 2001). These indices are based on species counts and
calculations on simple arithmetic formulas (Magurran, 2004). In
addition, they are easy to understand and a lot of data have already
been piled up contributing to water quality assessment. The results
have been presented in a previous review (Karydis, 2009). Twelve
ecological indices were tested but only three showed consistency in
detecting eutrophic trends: species number, total number of indivi-
duals and Kothe's species deficit. The Kothe's species deficit index
(Karydis and Tsirtsis, 1996) has been proposed to express the species
deficit between a discharge area and a reference sampling point
(control site). Shannon's index the most popular ecological index in
community ecology (Digby and Kempton, 1987) did not respond to
eutrophic levels.
In a recent work (Spatharis and Tsirtsis, 2010) on the development
of an ecological quality scale based on phytoplankton, 22 ecological
indices were tested for monotonicity using simulated data. Only
Margalef's, Menhinick's and Evenness E1 indices increased monoton-
ically. Margalef's index is a measure of species richness and is based
on the presumed linear relation between the number of species and
the logarithm of the number of individuals. Menhinick's index is also
a well-known index expressing species richness and was proposed
because it shows smaller sample variation compared to Margalef's
index. Evenness E1 expresses the degree of equality in species
abundance in the sample. A detailed description of these indices can
be found in Washington (1984), Karydis and Tsirtsis (1996) and
Magurran (2004).
The indices of Simpson's, Shannon's H′ and D′, Hill N1 and N2,
Hulbert's and McIntosh (Simpson, 1949; Washington, 1984; Magurran,
2004) did not show monotonicity but a characteristic hump-shape
curve instead (Spatharis and Tsirtsis, 2010). These indices increase at
low abundance values (less than 104 cells/l) and gradually decrease
reaching their minima at very high abundance values. Spatharis
and Tsirtsis (2010) further evaluated which of these indices were
showing linearity. They found that only Menhinick's and Evenness
Indices E2, E3 and E6 fulfilled both criteria: monotonicity and linearity. A
further step was to propose a composite index based on phytoplankton
metrics that is the sum of chlα concentration, abundance and diversity.
This index was called by the authors Integrated Phytoplankton Index
(IPI). Although the authors do not justify why the three variables of
the above metrics have equal weights, future applications will show
the effectiveness and credibility of the IPI Index.
Multimetric eutrophication indices have also been proposed by
Vollenweider et al. (1998) and Primpas et al. (2010). Vollenweider's
Index known as the TRIX index is a linear combination of four variables
(chlα, dissolved inorganic nitrogen, total phosphorus and the absolute
percentage of deviation of oxygen from oxygen saturation values).
 D. Kitsiou, M. Karydis / Environment International 37 (2011) 778–801
A eutrophication scale was also proposed mainly based on data
from the Adriatic Sea and was implemented in the national legislation
of Italy for the protection of water quality (Parlamento Italiano, 1999).
TRIX was also widely used for assessing eutrophication in the Black
Sea (Moncheva et al., 2001), the Caspian Sea (Nasrollahzadeh et al.,
2008; Shahrban and Etemad-Shahidi, 2010), the Persian Gulf (Taebi
et al., 2005), the Montego Estuary (Salas et al., 2008), the Southeast
Mexico (Herrera-Silveira and Morales-Ojeda, 2009) and the Helsinki
Sea (Vascetta et al., 2008). However, there are some drawbacks
concerning the suitability of the index reported in literature (a) the
TRIX index does not conform with the requirements of the Water
Framework Directive, WFD, 2000/60/EC (EC, 2000) as the scale is
not normalized to local reference conditions and physical, chemical,
biological variables are built-in within the index, although the
Directive requires interaction of separate evaluations of the above
mentioned variables (Pettine et al., 2007) and (b) in shallow coastal
waters dominated by macroalgal and phanerogam taxa, the use of
benthic indices is more appropriate as phytoplankton biomass
is negligible to describe nutrient effects (Giordani et al., 2009). In
recent work by Primpas and Karydis (2010b) it was attempted to
rescale TRIX index using oligotrophic waters as reference conditions
(Primpas and Karydis, 2010a).
Another multimetric index was proposed by Primpas et al. (2010)
and was found efficient in discriminating oligotrophic, mesotrophic
and eutrophic water types. Four nutrient variables and chlα concentra-
tions were used from three standard sets of data (Ignatiades et al., 1992)
characterizing eutrophic, mesotrophic and oligotrophic water types.
The form of the Eutrophication Index (E.I.) proposed is:
E:I: = 0:297CPO4 + 0:261CNO3 + 0:296CNO2 + 0:275CNH3 + 0:214CChlα
where C: nutrient and chlα concentrations.
The coefficients derived from the PCA analysis of the first Principal
Component. The index was validated using historical data from the
coastal area of Rhodes (Karydis, 1996) and the results were in
agreement with previously published work (Karydis, 1992; Moriki
and Karydis, 1994; Karydis, 1996). This index was also adapted to a
five level scale to be compatible with the requirements of the
European Water Framework Directive (a) less than 0.04: High quality
(b) 0.04–0.38: Good (c) 0.38–0.85: Moderate (d) 0.85–1.51: Poor and
(e) greater than 1.51: Bad.
Shallow coastal ecosystems are often dominated by extensive and
dense seagrass formations that use considerable amounts of nutrients
from the water column and the sediment. Nutrient uptake by
phytoplankton, micro and macro algae promotes algal growth and
finally seagrass can be replaced by opportunistic macroalgae (Zaldívar
et al., 2008a). At the same time benthic organisms are affected by
changing of the conditions in both, sediment and water column. The
study of the invertebrate community structure provides valuable
information on water quality since these organisms have long life
spans, they are characterized by different life cycles and they respond
to anthropogenic stress (Pearson and Rosenberg, 1978). They are
therefore suitable for assessing environmental quality (Elliot, 1994)
and a number of benthic indices have been developed for assessing
trophic status. The Ecological Evaluation Index (EEI) is based on
microalgal and phanerogam taxa (Orfanidis et al., 2001, 2003). The EEI
index scale ranges from 2 to 10 and expresses the ecological quality of
transitional and coastal waters, classifying the ecosystem quality from
high to bad. Seaweeds and seagrasses are the bio indicators of the
ecosystem and cover the range from reference conditions to the
last phase dominated by opportunistic species. The macrobenthos
indicator AMBI (biotic index), has been proposed by Borja et al.
(2000). This index was designed to characterize the ecological quality
of European coastal waters assessing the response of soft-bottom
macrobenthic communities to changes in water quality. The M-AMBI
is an indicator combining AMBI with Shannon's diversity (Borja et al.,
783
2003; Bald et al., 2005). The BENTIX index has been proposed by
Simboura and Zenetos (2002). It is based on macrozoobenthos soft
substrate and it is suitable in assessing ecological quality status
according to the requirements of WFD. The species are classified
into three ecological groups according to their response to organic
pollution. The ISD index was developed by Reizopoulou and
Nikolaidou (2004). It is based on a taxonomic free method, using
the distribution of the individuals of benthic communities on biomass
size classes. The skewness of the distribution is the measure of
community disturbance. All these benthic indices are also described in
detail by Zaldívar et al. (2008a).
A number of indicators have also been proposed for lake waters, a
long time ago (Vollenweider, 1969, 1976). Kirchner and Dillon (1975)
have developed empirical formulas to assess lake eutrophication
based on the relationships between phosphorus and chlorophyll
concentrations. Carlson (1977) proposed a Trophic State Index (TSI)
that could be calculated from several variables including Secchi disk
transparency, chlorophyll and total phosphorus. Although simple and
practical, TSI is based on a number of assumptions that make doubtful
the use of the index on a worldwide scale. Nevertheless indices based
on phosphorus–chlorophyll relationships are limited to freshwater
environments since it is known a long time ago (Dugdale, 1967) that
nitrogen is the limiting nutrient in the marine environment.
Information on ecosystem quality can be provided by the domi-
nance curves. A dominance curve is a graphical representation of a
community structure. The “dominance curve is based on a ranking
of species (or higher taxa) in a sample, in decreasing order of their
abundance or total biomass” (Clarke, 1990). The “alternative to these
dominance curves is to plot cumulative ranked abundances against
log species rank, as is so called ‘k-dominance’ curves” (Clarke, 1990).
Lack of equitability and domination of the community by few species
is illustrated by a steep curve. Dominance curves have been used
widely in benthic studies (Lambshead et al., 1983; Clarke, 1990), but
applications on phytoplankton data are rare. Ignatiades and Karydis
(1990) have used this method successfully to study seasonality in a
coastal marine environment.
The use of integrated indicators seems to be more appropriate for
detecting eutrophication trends. The search for eutrophication indices
to describe ecosystem change, considers oxygen budgets, transpar-
ency and chlorophylls as effect variables whereas, nutrients in rivers
should be preferably used as pressure indicators (Baan and van
Buuren, 2003). The use of phytoplankton indicators (pigment
measurements) and the coupling of these measurements with remote
sensing imagery as well as the use of ferries for automated water
quality monitoring have been proposed by Paerl et al. (2007).
The large number of indicators for assessing eutrophication
mentioned above is due to a number of reasons: (a) Different types
of ecosystems require specific field information (physical, chemical,
biological and geological variables) and maybe the use of specific
indices, (b) more complex indices have become popular over the last
two decades as they seem to be useful in coastal management studies
where integrated information is needed.
6. One-dimensional statistical analysis
One-dimensional statistical analysis methods used for quantitative
assessment of eutrophication are presented in this section along with
their objectives, advantages and shortcomings in eutrophication
studies. A concise presentation is given in Table 1.
6.1. Descriptive statistics
Numerical descriptive measures are the first step to summarize
data in statistics. The two mostly used descriptors are the central
tendency and the variability. Central tendency is usually expressed by
the mean and variability by the standard deviation. Variability is also
784 D. Kitsiou, M. Karydis / Environment International 37 (2011) 778–801

Table 1
One-dimensional statistical analysis methods used for quantitative assessment of eutrophication. Objectives, advantages and shortcomings in assessing eutrophication are provided.

One-dimensional Method objectives in eutrophication Advantages Shortcomings References

statistical methods studies

Descriptive Provides an overview of the Simplicity; it can be applied to Summary statistics does not provide Ignatiades et al. (1992)
statistics eutrophication state in an area. any kind of data describing any conclusive evidence concerning Hare and Mantua (2000)
Detection of regime shifts. eutrophication. eutrophication status.

Frequency FD illustrate the profile of nutrient Simple to apply development of Normality pre-requisite for probabilistic Ignatiades et al. (1992)
distributions (FD) and chlα values and form the basis scales for assessing eutrophication applications is not usually fulfilled. Giovanardi and Tromellini (1992)
for scaling eutrophication status. levels. Stefanou et al. (2000)

Outliers Outlying values express extreme
conditions of eutrophication.
Values expressing eutrophication
can be statistically detected.
Methodological limitations due to Karydis and Ignatiades (1992)
non-normally distributed nutrient Karydis (1994)
and chlα variables; limited use does
not allow method validation in
eutrophication studies.

Analysis of variance Eutrophication levels from different ANOVA is a well established ANOVA assumes normality not usually Tsirtsis and Karydis (1998)
(ANOVA) sampling sites can be compared. method; differences are detected met in nutrient and chlα variables;
at statistically significant levels. fairly often the data are pseudo-
replicates.

Correlation and The methods help to understand the Easy to apply; they contribute to Normality required; data transformation Ignatiades et al. (1987)
regression interaction between variables. the understanding of functioning distorts the natural information of the Nikolaidis et al. (2006)
among variables. system.

expressed by the variance and coefficient of variation. Minimum–
maximum values are also useful to define the lower and upper limit of
the physical quantity under study (Fowler et al., 1998). Summary
statistics is the first step in data handling prior to the application of
any data analysis techniques (Ignatiades, 2002a) but can also provide
information of the trophic status in an area if eutrophication scales
are available (Ignatiades et al., 1992; Stefanou et al., 2000). This
information is based on nutrient concentrations, chlα values,
phytoplankton cell number (cells/l) and water transparency. The
ASD (Average Standard Deviates) method (Ebbesmeyer et al., 1991) is
a popular method representative of those based on simple heuristics
rather than an underlying statistical model. The ASD was used to
detect regime shifts in the North Pacific in 1977 and 1989 (Hare and
Mantua, 2000). However, the ASD approach requires an a priori
specification of a regime shift date. Mantua (2004) gives a detailed
description of the application of the method for diagnosing regime
shifts. The Recurrence Quantification Analysis (RQA), a non-linear time
series analysis technique, based on Recurrence Plots (RP) has been
proposed by Zaldívar et al. (2008b) for the characterization of regime
shifts in environmental time series. This method is independent of
limitations such as data set size, data stationarity, and statistical
distributions of data. RQA is able to produce results with a low number
of data points. In addition, when compared to other statistical
techniques, it could be used for a fast screening of the data sets and a
combination with other techniques should follow (Andersen et al.,
2006b). Zaldívar et al. (2008b) presented three case studies regarding
regime shifts in different marine environments; lake eutrophication by
excessive phosphorus, regime shift in Ringkobing Fjord, Denmark and
oxygen dynamics in the Mediterranean coastal lagoon Sacca di Goro in
Italy. The results showed that for the detection of a single threshold in a
time series, RPs are robust against high noise levels (up to 100%). RQA
can be useful for the quantification of the results from RPs.
6.2. Frequency distributions
The frequency distribution of water quality variables has been a
research objective by field workers a long time ago (Heyman et al.,
1984). Most of the variables related to eutrophication follow the log-
normal distribution but fitness of some variables to beta and gamma
distributions has also been found (Ignatiades, 2002a). Fitting field
data to a known frequency distribution provides the experimenter
with two options: (a) to use the distribution as a probabilistic system
and assess water quality of an area under investigation using a limited
number of samples and examine the possibility of exceeding a critical
value and (b) knowing the distribution function of the data, is easy
to transform the data to normality and therefore be able to use
parametric statistical methods for further data processing. Standard
normal curves of nutrients have been developed by Ignatiades et al.
(1992) for assessing the trophic status. At the same time a similar
approach was also attempted by Giovanardi and Tromellini (1992)
using chlα concentrations. A simulated normal distribution of nitrate
concentrations has also been proposed by Stefanou et al. (2000). The
advantage of this procedure is that non-parametric data manipulation
methods were applied to define the central tendency and the dis-
persion of the distribution. Numerical applications of this “Physical–
Normal” distribution based on historical data showed that the
simulated normal distribution could be used as a standard curve for
eutrophication assessment studies on a probabilistic basis.
6.3. Outliers
An outlier could be defined as “an observation which deviates so
much from other observations as to arouse suspicions that it was
generated by a different mechanism” (Hawkins, 1980). There are two
mechanisms that lead to genesis of outliers; according to the first
mechanism the data come from heavy tailed distribution such as a log-
normal distribution. The second mechanism assumes that the data
arise from two distributions: the main or basic distribution that
generates “good observations” and the “contaminants distribution”
that generates “contaminants”. Extreme values on nutrient and
chlorophyll concentrations can be considered as values characterizing
eutrophic conditions. A summary statistics of the outlying values or
the number of outlying observations can be used as an estimate for
the trophic status. Only few outlying values may drastically shift the
mean to the right and broaden substantially the standard deviation.
It is generally advisable to remove the outliers before any statistical
analysis (Barnett and Lewis, 1994). The rejection procedure for
outliers is to “discard extreme order statistics whose deviation
from the remainder of the sample is sufficiently large” (Hawkins,
1980). Outlying values may be identified in frequency distributions,
regression models and multivariate data. However, in environmental
variables, possible identification of outlying values may indicate
extreme environmental conditions (Georgopoulos and Seinfeld,
1982), pollution problems or eutrophic trends. In those cases it is
 D. Kitsiou, M. Karydis / Environment International 37 (2011) 778–801
advisable to treat outliers as the values that express pollution effects
and therefore they should not be rejected as they carry information
related to ecosystem's stress. Outliers have to be used cautiously as
they may be the result of faulty sampling or poor analytical work.
However, frequent sampling in an area can show whether some
extreme values are a pollution episode or just faulty values. An attempt
was made to find out whether outliers could be an indicator of
eutrophic trends (Karydis, 1994). Nitrate, ammonium, phosphate and
chlα values derived from monthly sampling of ten stations spaced out
along the coastal area of the city of Rhodes, Greece, formed the data
basis. Outlying values were detected using the non-parametric box-
and-whisker plot; mean values of the outliers were calculated for each
station and cluster analysis was applied. Good discrimination of
clusters was observed among oligotrophic, mesotrophic and eutrophic
sampling sites. Outlying values (Karydis and Ignatiades, 1992) based on
phosphate concentration values were identified from nine stations in
Saronikos Gulf, Greece; it was found that the number of outlying values
was closely related to the proximity of the sampling sites to the sewage
outfall. Both papers indicated that outlying values could be used as a tool
for quantitative assessment of eutrophication. However, in spite of the
available statistical methodology, outliers have not been used in water
quality and marine pollution studies. An interesting application will be
the detection of outliers from multivariate data as eutrophication
processes are monitored and assessed through a number of variables.
6.4. Analysis of variance
Analysis of variance (ANOVA) is among the most popular, powerful
and versatile tools in natural sciences. It is a family of techniques
developed to compare the means of more than two populations.
Although they have been designed for planned laboratory experiments,
they are also suitable for field data concerning natural populations and
abiotic parameters. The null hypothesis is the equality of means.
Although the hypothesis generation in ANOVA seems to be simple,
Underwood (1981) in an extensive review of ANOVA techniques
applied in the fields of marine biology and ecology, states that in spite
of the widespread use of the ANOVA methodology, serious problems
have risen in “the use (and abuse)” of analyses of variance possibly
because of insufficient understanding of the methods by the workers.
The reasons may be violations of the assumptions (normality and
equality of variances), poor experimental design and erroneous
conclusions. Underwood investigated 151 papers and found that
most of the problems were located in the presentation, computation
and interpretation of the analyses.
Depending on the number of factors under comparison as well as
on the experimental design, analysis of variance can be one-way, two-
way, three-way, multifactor ANOVA, nested design and split-plot
design (Sokal and Rohlf, 1981). Application of one way analysis has
been reported for testing the effect of depth (one factor) on both
nutrients as well as chlα (Ignatiades, 1990). The same author has
also applied two way ANOVA for testing the effects of station and
season on phytoplankton abundance (Ignatiades et al., 1995) as well
as the effect of three factors (season, station and depth) on chlα
concentrations (Ignatiades, 1998). The statistical distinctness of ANOVA
in assessing differences of the trophic status between sampling stations
was investigated recently (Primpas and Karydis, 2010a). Historical data
were used from 9 sampling sites in Saronikos Gulf, Greece, influenced by
the sewage outfall of Athens. Raw data, transformed data and simulated
data of nutrients, chlα and phytoplankton cell number (cells/l) were
tested. The pairwise comparisons followed after the application of
the ANOVA, showed that the simulated data were highly sensitive in
detecting differences between stations. The pairwise multiple compar-
ison procedures have been reviewed extensively (Jaccard et al., 1984;
Day and Quinn, 1989). Both papers deal with the problem of violation of
assumptions especially variance heterogeneity and normality. Day and
Quinn (1989) proposed parametric and no parametric methods of
785
pairwise comparisons and many recommendations are given regarding
ecological data. However, in spite of the extensive literature on pairwise
tests, there are not many applications on nutrient and phytoplankton
variables (Underwood, 1981; Underwood, 2007) and therefore the
efficiency of those methods in assessing eutrophic levels cannot be
evaluated. Phytoplankton richness and abundance have been statisti-
cally evaluated in transitional waters in the Mediterranean (Vadrucci
et al., 2008). Spatial differences of both cell abundance and species
richness were assessed using two-way nested ANOVA. The results
showed that cell density was significantly affected by temperature
changes. ANOVA was also applied to evaluate 20 phytoplankton indices
for detecting eutrophic trends (Tsirtsis and Karydis, 1998).
6.5. Correlation and regression
The association between variables is studied by the correlation
analysis. On the other hand the study of the functional relation between
a variable (or variables) known as independent variable(s) over one
dependent variable is performed through regression analysis (Sokal
and Rohlf, 1981). The two methods are based on similar mathematical
relations and quite often a correlation problem is treated as regression
or vice versa. According to Sokal and Rohlf (1981) the data available for
the analysis by the investigator may not be appropriate for one or the
other method.
In correlation analysis there is no distinction between dependent
and independent variables but are both influenced by the same
factor. The product moment correlation is the most commonly used
correlation in statistics among numerous correlation coefficients. There
are many applications of correlation between nutrients (phosphate,
nitrate and ammonia) and phytoplanktonic variables (chlα, species
richness and cell number). The relationship among phytoplankton cell
density, total carbon and chlα has been used to understand aspects of
phytoplankton ecology in the Northern Adriatic (Revelante and
Gilmartin, 1995). When chlα or phytoplankton biomass is correlated,
the observed correlation may be influenced by: (a) nutrient variables
(b) physical variables (temperature and transparency) and (c) chance
fluctuations or other unknown variables. In that case partial correlations
and partial covariances are very useful as the correlation due to (a) and
(b) is removed leaving only the correlation due to phytoplankton
variables as well as unmeasured ecosystem variables (Poole, 1974). An
application of partial correlation in marine phytoplankton communities
has shown that the partial correlation coefficient between dark fixation
and the ratio productivity/biomass was higher than the simple
correlation due to correction by the nutrient and cell density variables
of the matrix (Ignatiades et al., 1987). Correlation coefficients do not
seem to be statistically significant in oligotrophic marine environments
(Vounatsou and Karydis, 1991): the limited number of statistically
significant relationships between chlα and nutrients was attributed by
the authors to a number of problems arising from the very low values
including high analytical errors and shortcomings from data handling as
well as to the facts that vitamins and trace metal concentrations that
play a critical role in oligotrophic waters are not measured in routine
field work. Many other variables or processes (oxidation of organic
matter, turbulence and changes due to upwelling movements) also
affect nutrient and phytoplankton concentrations but they are rarely
taken into account. On the contrary in mesotrophic and eutrophic
waters nutrient and phytoplankton variables showed strong correla-
tions (Ignatiades et al., 1985).
The relationship between the dependent and the independent
variable(s) in a regression model may be (a) simple, (b) multiple or
(c) stepwise regression. Regression can also be linear or non linear.
These techniques have been described by Draper and Smith (1998).
Although the linear regression has been used extensively in
phytoplanktonic and eutrophication studies, mainly to study the
effects of nutrient on phytoplankton variables, it is doubtful whether
the researchers have always examined the very strict assumptions of
786 D. Kitsiou, M. Karydis / Environment International 37 (2011) 778–801
the simple linear regression (Poole, 1974). Multiple regression has
been applied by Estrada et al. (1993) to study the dependence of
primary production on chlorophyll, depth and water stability. The
main difficulty in applying multiple regression is the presence of
possible interactions among independent variables (Poole, 1974).
Each interaction accounts for an independent variable and therefore
the linear model becomes cumbersome and not easy to apply
especially with a limited number of observations.
In the stepwise linear regression, the independent variables Xi
are arranged in an order according to the proportion of the corrected
sum of squares of the variable Y they explain. An application of the
stepwise regression has been given by Vounatsou and Karydis (1991).
Chlα was the depended variable and was regressed over phosphate,
silicate, nitrate and ammonia. Reciprocal and exponential transforma-
tions were found most appropriate for good fitting of the model.
A piecewise linear regression model was applied to estimate the
concentration of chlα as a function of nitrates in water masses from
Themaikos Gulf, a eutrophic area in the Northern Aegean (Nikolaidis
et al., 2006).
Correlations of bloom indicators during different years with
nutrient concentrations have been carried out to detect regime shifts
and determine the threshold nutrient levels for harmful algal events in
some European coastal waters (Stolte and Graneli, 2006). In the same
study, trends were studied using linear regression. Autoregressive
Moving Average (ARMA) models and Vector Autoregressive (VAR)
modeling have been used to detect regime shifts in large marine
ecosystems (Mantua, 2004) when a collection of large ecological time
series is available. In the process of identifying regime shifts, there is
the risk of detecting thresholds which are just random fluctuations.
The use of statistical hypothesis testings aims at limiting this
possibility to a pre-determined fixed value, typically at a significance
level of 5%. If the time of the threshold event is known (e.g. change in
management practice) analysis of the significance probability of the
regime shift under the null hypothesis of no change can be carried out
using intervention methods (Box and Tiao, 1975). Nevertheless, this
approach cannot be adopted when the change-point occurs at an a
priori unknown time. Intervention analysis is attractive because it
allows a quantitative estimate of the statistical significance of step
interventions, while accounting for autocorrelation in the time series
of interest (Noakes, 1986). The Vector Autoregressive (VAR) modeling
approach provides an objective means for identifying and assessing
the statistical significance of regime shifts (Mantua, 2004).
Autocorrelation is a characteristic of data in which the correlation
between the values of the same variables is based on related objects.
Autocorrelation sometimes is referred to as serial correlation and
determines the presence of correlation between the values of variables
that are based on associated aspects.
The classical regression model includes an assumption about the
independence of the disturbances between consecutive observations.
If this assumption is violated the errors in one time period are
correlated with their own values in other periods and a problem of
strictly autocorrelated errors or disturbances arises. Cross-correlation
compares one series of data with another to identify and locate
positions of high correlation between two series.
Pagou and Ignatiades (1988) gave a detailed description of these
methods and applied them to detect seasonality patterns of phyto-
plankton in eutrophic marine coastal waters. The dynamics and
ecological significance of daily internal load of phosphorus in shallow
Lake Balaton, Hungary was supported by autocorrelation analysis
(Istvanovics et al., 2004). It was revealed that proper determination of
the suspended particulate matter (SPM) and the coefficient of vertical
light attenuation (K-d) required daily sampling; thus, routine
monitoring does not provide a thorough insight into environmental
variability of shallow lakes as habitats for phytoplankton. Verleyen
et al. (2004) aimed to quantify habitat-specific diatom production in
Antarctic marine sediments by detecting the correlation between
diatom pigments and diatom biovolume after correction for temporal
autocorrelation. In addition, autocorrelation was estimated during
testing of non-linear stochastic models on phytoplankton biomass
time-series, since it was considered as an important factor for the
accuracy of such models (Stollenwerk et al., 2001). Spatial autocor-
relation is discussed in Section 10 (Spatial analysis).
7. Multi-dimensional statistical analysis
Statistical methods for assessing eutrophication are based on a
limited number of variables describing eutrophication (nutrients
concentrations, phytoplankton, macrophyte biomass and water trans-
parency) or affecting plant biomass production (temperature). Raw
data usually require a preliminary data analysis (Fig. 1) so as to test
whether the assumptions of the statistical methods that could be
applied are satisfied or can be satisfied after data manipulation. The
outcome of the statistical methods mentioned in the present work can
provide a scale of the eutrophication state, detect eutrophication trends
and rank sampling sites according to the level of eutrophication. These
results can either be used as “end products” or can be assimilated in
more complex methods: multiple criteria choice techniques, spatial
methods. This information can contribute to various fields of application
such as coastal management, coastal water quality assessment and
environmental protection; it can also provide background information
for environmental legislation (International Conventions, EU Directives
and National Legislation).
The multi-dimensional statistical analysis methods used for
quantitative assessment of eutrophication are presented in Table 2
with their objectives, advantages and shortcomings in eutrophication
studies.
7.1. Principal Component Analysis (PCA)
Principal Component Analysis is a multivariate statistical method
that forms new variables which are linear transformations of the
original variables (Sharma, 1996). These new variables are uncorrelated
and represent a great percentage of the information of the original
variables. The main objective of the method is to reduce the
dimensionality of the initial set of data. It is much easier to understand
the uncorrelated variables than the complex and voluminous informa-
tion of the initial data matrix (Dunteman, 1989). This data compression
into a lower dimensional space is known as “dimensional reduction”.
This is why PCA is also characterized as a “dimensional reduction
technique” (Sharma, 1996). This method has been used in the past in
exploratory data analysis to assess the water quality of rivers and to
quantify anthropogenic influences (Vega et al., 1998); nutrients, oxygen
concentration, BOD and COD were among the variables of the data
matrix. However, these publications did not focus on eutrophication
but rather to a more general water quality assessment. Application of
PCA for assessing eutrophication has recently been published (Primpas
et al., 2010) in an effort to develop the multimetric index presented
in Section 5.
7.2. Cluster Analysis (CA)
Ecologists have collected quantitative information for more than a
century to assess the resemblance between the objects that is the sites
(sampling areas) and the variables describing them (species/species
abundance, indicators and abiotic variables). The quantification of the
association between sites and descriptors is the first step in numerical
analysis of ecological data (Legendre and Legendre, 2003). The second
step is the grouping of the objects according to their similarity. This
grouping is usually illustrated in the form of a dendrogram. Although
there are many books on clustering techniques (Pielou, 1984; Gauch,
1989; Sharma, 1996; Everitt et al., 2001; Legendre and Legendre, 2003;
Romesburg, 2004), there is still controversy concerning the efficiency
 D. Kitsiou, M. Karydis / Environment International 37 (2011) 778–801
Fig. 1. Flow chart of statistical procedures applied for quantitative assessment of eutrophication and fields of application.
of clustering methods in ecological and environmental applications
(Cao et al., 1997). The main reasons for these controversies are:
(a) criteria of choosing similarity (or distance) measures. The selected
algorithm can greatly influence the outcome of cluster analysis
(Ludwig and Reynolds, 1988). (b) The choice of clustering algorithms
(Everitt et al., 2001; Primpas et al., 2008). (c) Possible uncertainty
concerning the “structure” of the ecological data.
The choice of similarity measures is subjective and introduces
varying degrees of bias to the communities (Cao et al., 1997).
However, the choice has to be considered in the context of the
particular study, taking into account the nature of the data and the
intended type of analysis (Gower and Legendre, 1986). A group of
quantitative distance coefficients based on Euclidean measures
(Ludwig and Reynolds, 1988; Romesburg, 2004) seem to suit to
abiotic variables characterizing eutrophication such as water trans-
parency, nutrient concentrations, chlα values and phytoplankton
cell number. It has been reported (Cao et al., 1997) that the Euclidean
Distance overweights abundant species even after data transforma-
tion. The same trend has been observed in assessing eutrophication
using nutrient and chlα concentrations (Karydis, 1992). Among the
Euclidean measures used, the Absolute Distance d(j,k) = Σi|xij − xik|
seemed to provide the best resolution in the mesotrophic range; this
787
was explained by the fact that differences in nutrient and chlα values
were summed but not squared. The correlation coefficient also known
as Pearson Product-Moment correlation coefficient (Romesburg,
2004) is not recommended (Everitt, 1981); it has shown limited
resolution in defining discrete groups in sets of data. Canberra Metric
Coefficient and Bray–Curtis coefficient are appropriate only for
community analysis. The Bray–Curtis similarity coefficient has been
used extensively in ecological research (Magurran, 2004). A method
has been developed (Mumby et al., 1996) for introducing species
weights into the calculation of the similarity matrix. As weights
reflect the significance of a species in connection with a particular
ecosystem's trend, it is obvious that “species weighting” can be of
importance in eutrophication studies if toxic algae or species
indicators are present. The main criterion for choosing a clustering
algorithm for eutrophication assessment is to be successful in site
discrimination as well as in assessing different trophic conditions. In a
work on river macro invertebrates (Cao et al., 1997) four clustering
methods were tested: UPGMA (Average Linkage Clustering Method),
Ward Linkage, Compete Linkage and TWINSPAN. The Ward Linkage
was found as the most successful agglomerative algorithm in
discriminating tributaries. It was also found that TWINSPAN was an
effective divisive algorithm. Eight clustering algorithms were tested to
788 D. Kitsiou, M. Karydis / Environment International 37 (2011) 778–801

Table 2
Multi-dimensional statistical analysis methods used for quantitative assessment of eutrophication. Objectives, advantages and shortcomings in assessing eutrophication are provided.

Multi-dimensional Method objectives in eutrophication Advantages Shortcomings References

statistical methods studies

Principal Component The method points up the main variables Limits the number of variables related Mostly a preliminary method for Lundberg et al. (2009)
Analysis (PCA) influencing eutrophication trends. to eutrophication. eutrophication assessment. Primpas et al. (2010)
Detection of regime shifts. Easy to apply.
Easy to understand the outcome.

Cluster Analysis (CA) Classification of sampling sites based on Non-parametric. Limited access to tests of significance. Vassiliou et al. (1989)
variables describing eutrophication. Easy to understand the classification Different outcome (dendrogram) due Stefanou et al. (2000)
scheme. to different similarity measures and Primpas et al. (2008)
clustering algorithms.

Discriminant Identifies the variables that differentiate DA can illustrate different DA assumes normality. Tsirtsis and Karydis
Analysis (DA) sampling sites. eutrophication conditions. Not many applications in eutrophication. (1999)

Multi Dimensional MDS is a 2D presentation of sampling sites Non-parametric. Limited number of applications in Field et al. (1982)
Scaling (MDS) based on “proximities” between them. Methods for significance testing eutrophication studies. Karydis (1992)
available.
Easy to understand.

Correspondence The method is equivalent to PCA for Linearity is not required. Limited applications on phytoplankton Ignatiades et al. (1992)
Analysis (CA) non-metric data. ecology. Okolodkov and Dodge
(1996)

Gradient Analysis GA is applied to describe the distribution Useful for assessing eutrophication Not many applications in McQuoid and Hobson
(GA) of variables along natural gradients. levels in estuaries and sewage outfalls. eutrophication studies. (1997)

evaluate the efficiency in discriminating between oligotrophic,
mesotrophic and eutrophic sites (Primpas et al., 2008). The Ward's
algorithm showed the best resolution in discriminating sampling sites
of different trophic status. Clustering structure becomes more stable
with less possibility to be modified as a result of minor changes in data
values if high resolution coefficients are used (Hajdu, 1981). It is
therefore obvious that high resolution of the measure of similarity is a
desirable property in clustering (Gower and Legendre, 1986). Cluster
analysis as well as other multivariate procedures has been applied on
nutrient and phytoplankton data (Ignatiades, 2002b); however, the
results are lacking of statistical evaluation. In spite of the need for
research on tests of significance in cluster analysis that has been
emphasized a long time ago (Boelsch, 1977) there is a limited number
of attempts and even fewer applications. A quick randomization
algorithm has been developed, generating permutations on two
or three columns of the data matrix simultaneously at a level of
significance (Vassiliou et al., 1989).
7.3. Discriminant Analysis (DA)
Discriminant Analysis is applied on studies in marine ecology to
classify objects into groups. The procedure is based on several
variables. There are two advantages using DA: (a) parsimony of
description and (b) clarity of interpretation (Stevens, 1996). A
classification system for assessing eutrophication based on nitrate
phosphorus and chlα values using DA has been proposed (Tsirtsis and
Karydis, 1999). The three variables used for the estimation of the two
discriminant functions are given by the formulas:
Function 1 = 3:242–0:130V1 + 0:896V2 + 5:584V3
Function 2 = 1:081–0:378V1 + 2:932V2 + 3:211V3
where V1, V2 and V3 are the logarithms of nitrate, phosphate and
chlorophyll concentrations. The two functions were used to plot a
territorial map divided into three defined regions, a eutrophic, a
mesotrophic and an oligotrophic field. Any unknown samples can be
plotted and assessed using this map.
7.4. Multidimensional Scaling (MDS)
Multidimensional Scaling is a method designed to construct a
graph usually in two dimensions showing the relationships between
many objects once the triangular table of distances has been given
(Manly, 2001). The method has been widely used since the 80s in
analyzing multispecies patterns (Field et al., 1982) and benthic
marine studies (Warwick et al., 1988). Although MDS is a useful
method as a non-metric procedure, it can be supported by an ANOSIM
test (analysis of similarities) that provides statistical significance. The
applications in eutrophication studies are limited (Karydis, 1992;
Moriki and Karydis, 1994).
7.5. Correspondence Analysis (COA)
This method examines the relationship between samples and
species by simultaneous ordination (Pielou, 1984; Ludwig and
Reynolds, 1988). Work on COA has been published on phytoplankton
ecology but without reference to eutrophication (Ignatiades et al.,
1992; Okolodkov and Dodge, 1996).
7.6. Gradient Analysis (GA)
Gradient analysis includes methods on arranging physical, chemical
and biological variables in an increasing or decreasing order. Although
gradient analysis is a well structured methodology popular among
terrestrial botanists (Whittaker, 1982), it can be also particularly useful
in describing eutrophic gradients in the coastal marine environment.
However, there are only few applications on phytoplankton (McIntire,
1978; McQuoid and Hobson, 1997).
8. Multiple Criteria Analysis (MCA)
MCA is an evaluation method that provides the means for ranking
a number of hypotheses known as alternative choice possibilities,
using a number of multiple criteria and conflicting objectives (Voogd,
1983; Nijkamp and Voogd, 1986). A MCA method combines a ranking
algorithm and a criteria weighting method. Criteria can be expressed
in both metric and non-metric form and are of crucial importance for
the evaluation of the results. Furthermore, weights can be assigned to
 D. Kitsiou, M. Karydis / Environment International 37 (2011) 778–801 789

criteria to represent their relative importance, either in cardinal or
ordinal units.
A wide range of methods and procedures are available within the
framework of MCA for designing, evaluating and prioritizing alterna-
tive decisions (Malczewski, 2006). However, all of them obey the same
principle: the pairwise comparison of the scores for all the alternatives
and for each criterion (Nijkamp and Voogd, 1986). On the other hand,
there is a number of weighting algorithms for expressing criteria
importance, ranging from simple direct methods — equal weights
method and rank-order weighting method — to more complex
approaches. The application of any MCA method is a stepwise
procedure that involves the following steps: (i) determination of the
hypotheses or alternative choice possibilities, (ii) selection of the
appropriate evaluation criteria, (iii) creation of the Impact Matrix,
(iv) standardization of the Impact Matrix, (v) assignment of weights
to the criteria based on an appropriate weighting algorithm,
(vi) application of an appropriate ranking or scoring algorithm to
rank the alternative choice possibilities.
The Impact Matrix can have the following form when, i hypotheses
and j criteria are considered:
method (Voogd, 1983) separates quantitative (cardinal) and qualita-
tive (ordinal) data in the Impact Matrix, applying appropriate
algorithms to each level of measurement. A detailed description of
the method is given by Hajkowicz and Higgins (2008).
ELECTRE methods, such as ELECTRE II, III and IV are widely known,
as the concordance approaches. Concordance analysis focuses on the
notion of concordance that is the degree to which one alternative
performs better than another. A dominance relationship for each pair
of alternatives is derived using both an index of concordance and an
index of discordance. ELECTRE methods are described in detail by
Wang et al. (2009).
The Regime method is considered as an ordinal generalization of
pairwise comparison methods. It uses a random generator to estimate
for each pair of alternatives the probability that one alternative ranks
above another. A detailed description of this method is given by
Janssen (1992).
MCA methods have been proved very useful in assessing eutrophi-
cation trends (Table 3) in coastal areas and are therefore frequently
included in methodologies related to coastal management and decision-
making (Linkov et al., 2006; Hajkowicz, 2007; Ananda and Herath,
2009). Regime method has been applied in assessing coastal marine

j j
b11 … b1j eutrophication problems (Moriki and Karydis, 1994) and proved
Impact Matrix = b21 … b2j effective for the discrimination of trophic status in coastal areas.
bi1 … bij Almasri and Kaluarachchi (2005) presented an integrated metho-
dology for the optimal management of nitrate contamination of
where bij is the score of the hypothesis i according to the criterion j. In ground water by combination of environmental assessment and
the case that b1j N b2j, the hypothesis I1 dominates over the I2 as far as economic cost evaluation. A MCA application for mapping the risks
the j criterion is concerned (Hartog et al., 1989). of agricultural pollution for water resources has been applied by
Numerous MCA methods are available in the literature. The Giupponi et al. (1999) by incorporating soil and climate variables
Weighted Summation (WS) is the most popular and commonly and alternative land uses in the Impact Matrix. In Koo and O'Connell
applied MCA method because it is characterized by simplicity and (2006) an integrated modeling and multi-criteria analysis was
reliability of the results (Howard, 1991; Janssen, 2001). The Evamix applied to evaluate a set of land use alternatives and to identify an

Table 3
Multiple criteria analysis, remote sensing, spatial analysis, mapping, modeling used for the quantitative assessment of eutrophication. Objectives, advantages and shortcomings in
assessing eutrophication are provided.

Methods Method objectives in eutrophication Advantages Shortcomings References

studies

Multiple criteria Ranking of sampling sites/study
analysis (MCA) areas according to their
eutrophication level based on
various criteria/variables.
Assignment of weights to the criteria. Optimal selection of variables is needed. Janssen (1992)
Co-estimation of variables of different Subjective nature, especially during the Kitsiou et al. (2002)
origin. weighting procedure. Malczewski (2006)
Distribution free method. Optimal choice of the weighting method
is important.

Remote sensing Eutrophication level of coastal
areas at spatial scale and analysis
of the observed trends.
Eutrophication assessment at large
spatial scales.
Available datasets even though
in situ data are not available.
Operation only on the sea surface skin. Maritorena and Siegel
Clouds can hamper the transmission of (2005)
electromagnetic radiation. Garcia et al. (2005)
Lack of satellite data of very high
spatio-temporal resolution.

Spatial analysis Description and analysis of the Calculation of specific statistics which Deep knowledge of the methods is required Cliff and Ord (1973)
spatial structure of data. are expressed as graphs; better in order to reach accurate conclusions, Legendre and Legendre
Detection of eutrophication trends understanding, evaluation and analysis especially in the case of variograms. (2003)
based on the study of anisotropies of the results.
and the degree of homogeneity in
the study area.
Optimization of sampling design.

Mapping Study of the spatial distribution of
variables related to eutrophication.
Illustration of eutrophication trends
on thematic maps.
Conversion of the fragmented
information of in situ datasets
into smooth gradient of data values.
Selection among various methods
of interpolation.
Accuracy depends on the initial dataset Lam (1983)
from in situ measurements. Burrough and McDonnell
Effective selection of the appropriate (2000)
interpolation method.
Deep knowledge of the interpolation
methods is required.

Modeling Forecast of eutrophication trends.
Explore relationships between
causes and effects of eutrophication.
Detection of regime shifts.
Fills data gaps.
A variety of modeling approaches are
available to describe eutrophication
dynamics.
Useful for the evaluation of
management alternatives.
Unrealistic to create a single model to Rast et al. (1983)
address all the interactions among variables. National Academy of
Calibration of models is based on data sets Sciences (2003)
from a specific location. Zaldívar et al. (2009)
Quite complex approach.
790 D. Kitsiou, M. Karydis / Environment International 37 (2011) 778–801
‘ideal’ compromise between economic return and environmental
pollution.
9. Remote sensing
Estimation of the eutrophication level of coastal areas and analysis
of the observed trends, especially at large spatial scales, are not
always effective if they are limited on classic oceanographic sampling
campaigns. During the last decades, the contribution of remote sensing
to coastal eutrophication assessment has been invaluable (Table 3).
Ocean color is a unique property, measured from satellite sensors to
provide information on oceanographic parameters from the sea
surface to a few tens of meters depth (Maritorena and Siegel, 2005).
Most of the quantitative applications of ocean color remote sensing to
assess eutrophication trends have focused on the estimation of
abundance and distribution of phytoplankton chlorophyll in the
seawater; therefore, surface patterns of phytoplankton biomass
distribution at large spatial scales are provided (Garcia et al., 2005).
Data from various satellite sensors have been used in studies related
to coastal eutrophication. CZCS was the first instrument devoted to
the measurement of ocean color, especially chlorophyll concentrations
(Iverson et al., 2000). Landsat MSS/TM/ETM+ and SPOT sensors have
also provided valuable information on coastal eutrophication studies
(Torbick et al., 2008). However, the launch of SeaWiFS in 1997 followed
by MODIS/AQUA and MERIS in 2002 made available a huge set of ocean
color data (Vos et al., 2003; Gons et al., 2008; Werdell et al., 2009).
Numerous studies are found in the literature where satellite data are
used to assess eutrophication problems in coastal areas. Gohin et al.
(2008) used SeaWiFS satellite data and classified the coastal waters of
the French Atlantic continental shelf and the English Channel following
the eutrophication risk criterion of the Water Framework Directive
(WFD). Monitoring of HABs (Harmful Algal Blooms) by targeting
specific species and time period (generally spring and summer) when
conditions for remote observation are most favourable (Miller et al.,
2006) has also been carried out. Shevyrnogov and Vysotskaya (2006)
studied the spatial distribution of chlorophyll concentration based on
the autocorrelation analysis of SeaWiFS data.
In addition, numerous approaches have been performed to develop
optimum algorithms from satellite data sets to predict the concentra-
tions of variables related to coastal eutrophication. Kabbara et al.
(2008) presented derived empirical algorithms to estimate chlα
concentration, Secchi disk depth and turbidity of coastal waters from
the combination of ETM+ imagery and in situ data in the coastal area
of Tripoli, Lebanon. In literature, an extended description of specific
algorithms applied to determine the concentration of variables related
to eutrophication can be found focusing on specific characteristics of
coastal waters (Gitelson, 1993; Chavula et al., 2009).
10. Spatial analysis
Spatial analysis provides the means for the description of the
spatial structure and the heterogeneity in data. Spatial analysis can be
carried out in the framework of a GIS that is a powerful spatial data
processing system (Huang et al., 2001) capable of storing, managing
and analysing spatially referenced data (Burrough and McDonnell,
2000). GIS has been widely used for the creation of accurate spatial
databases and maps and the processing and analysis of environmental
data sets (Jankowski, 2009).
In spatial pattern analysis, which deals with the study of spatially
continuous phenomena such as coastal eutrophication, heterogeneity
refers to variations in the measurements collected through sampling
at discrete sampling sites. Spatial structures can be described through
structure functions which allow the quantification of the spatial
dependency and its partitioning among distance classes (Legendre
and Legendre, 2003). Correlograms and variograms are the most
commonly used structure functions.
Fig. 2. The variogram and its parameters: the range, the sill and the nugget variance.
Spatial correlogram is a graph where autocorrelation values are
plotted in y-axis against distance classes among sampling sites. Spatial
autocorrelation can be measured by either Moran's I or Geary's c spatial
autocorrelation statistics (Cliff and Ord, 1973). A detailed description of
spatial correlograms is given by Legendre and Legendre (2003).
The variogram (Fig. 2) is the basic tool of geostatistics and provides
a mathematical description of the relationship between the variance
of pairs of observations and the distance separating them (Mabit
and Bernard, 2007); therefore, it is frequently used for the detection
of anisotropies and the determination of the degree of homogeneity
in a study area (Vázquez et al., 2005). Anisotropy is present in data
when the autocorrelation function is not the same for any geographic
direction. The variogram is expressed as a graph where the semi-
variance γ(h) is plotted in y-axis against distance classes among
sampling sites. The semi-variance γ(h) is an autocorrelation statistic
given by the formula,
1 n
2
γðhÞ = ⋅ ∑ fZ ðxi Þ−Z ðxi + hÞg
2n i = 1
where Z(xi) is the value of the examined variable at the position xi,
Z(xi + h) is the value of the examined variable at the position xi + h
and n is the number of pairs of observations separated by distance
h, called lag (Fig. 2).
The sill, the nugget variance, the scale and the range are the most
important parameters of a variogram. The sill is the maximum
attained value of γ(h) indicating that there is no more spatial
dependence in data and corresponds to a specific separation distance
among sampling sites, called range. The nugget variance represents
the semi-variance value γ(h) when h = 0. It corresponds to the local
variation occurring at scales finer than the sampling interval and it is
also related to the measurement and sampling error. The ‘nugget-to-
sill’ ratio is an important indicator of the spatial dependence of a
variable (Cambardella et al., 1994).
Directional correlograms and variograms can be calculated to
study the spatial structure of a variable at a specific direction. In
addition, the surface variogram is represented as a pixel map and is
used to determine whether anisotropy is present in the data and to
indicate with precision the directions where different degrees of
anisotropy are observed (Michelakaki and Kitsiou, 2005).
Spatial analysis methods have been widely applied in assessing
coastal eutrophication (Table 3). An assessment of the spatial processes
in ecological data has been carried out by Blanchet et al. (2008) who
proposed that gradients influencing species spatial distributions can be
studied via spatial variables that represent directional spatial processes.
Autocorrelation analysis has been also applied on a data set derived
 D. Kitsiou, M. Karydis / Environment International 37 (2011) 778–801
from SeaWiFS satellite data and a pronounced heterogeneity of the
spatial distribution of chlorophyll concentration seasonal dynamics has
been revealed. Finally, spatial autocorrelation has been used for the
planning of ecological experiments, since a variable could be charac-
terised as homogeneous or heterogeneous in space regarding the scale
at which it is studied (Dutilleul, 1993; Legendre, 1993).
Geostatistics have been applied by Anttila et al. (2008) to
investigate patchiness of water quality related to sampling metho-
dology with the aim to develop an optimal sampling network. The
development of an optimal sampling design for eutrophication studies
has also been reported by Kitsiou et al. (2001); 34 sampling sites
used for chlorophyll concentrations were located in a grid pattern
(1 × 1 NM), in the Strait of Lesvos, Greece, forming the source of
data. These sampling sites were reallocated by taking into account
optimized sampling strategy (Mason et al., 1989) and anisotropy of
chlorophyll concentrations using variograms. This way, variance
fluctuations were reduced over a heterogeneous area. Eleveld and
van der Woerd (2006) carried out semi-variogram analysis to a data
set of chlorophyll and suspended particulate matter derived from
SeaWiFS satellite data in order to investigate their variability in the
study area and assess the range where the measurements become
independent. Finally, Flipo et al. (2007) assessed the nitrate pollution
by combining geostatistics and physically based modeling.
11. Mapping
In two-dimensional space, the spatial structure of a variable can be
visualized by maps that illustrate its spatial distribution (Table 3).
Interpolation methods provide the means for the creation of surfaces
from irregularly spaced point data by converting the fragmented
information collected during sampling surveys into a smooth gradient
of data values (Burrough and McDonnell, 2000). There are a number
of alternative interpolation methods for creating such surfaces, and
they are grouped in two general categories: the global and the local.
Global-fit procedures calculate a single function describing a surface
that covers the entire map area. Local-fit procedures estimate the
surface at successive nodes in the grid using only a selection of the
nearest data points. An extended review of the available interpolation
methods can be found in Lam (1983) and Li and Revesz (2004). Trend
surface analysis, also called trend surface mapping, is the most widely
used global surface-fitting procedure (Lancaster and Salkauskas,
1986). Inverse Distance Weighted (IDW) methods are based on the
assumption that the interpolated values of a variable are more
influenced by the nearby observations than those located in a greater
distance. The interpolating surface is a weighted average of the scatter
points and the weight assigned to each scatter point diminishes as the
distance from the interpolation point increases (Weber and Englund,
1992; Weber and Englund, 1994). Kriging is an interpolation method
and a fundamental tool in the field of geostatistics. Kriging is based on
the assumption that the variable being interpolated can be considered
as a localized variable (Matheron, 1963). Kriging is a local interpolator
and is based on the analysis of variograms to estimate the spatial
structure of the variable under study and calculate optimum weights
at each sampling distance (Isaaks and Srivastava, 1989; Cressie, 1993).
Legendre and Fortin (1989) showed the major importance of the
study of the spatial autocorrelation of biological parameters using a
combination of correlograms and interpolation methods for develop-
ing thematic maps. Li and Reynolds (1994) considered that the
quantification of the spatial heterogeneity of biological parameters
illustrated on thematic maps is of principal interest for assessing the
structure of the system under examination. Newton et al. (2003) in
their study to evaluate eutrophication in the coastal lagoon of Ria
Formosa, Portugal, used the IDW method to interpolate the available
data sets of a number of related parameters and produce maps. White
et al. (2004) examined the spatio-temporal patterns of nutrient and
chlα concentrations in two shallow well-mixed estuaries using GIS
791
plots. Cruzado et al. (2002) assessed the nutrient fluxes from the
Ebro River and subsequent across-shelf dispersion for assessing the
environmental quality of the coastal zone; mapping of the vertical
distributions of relevant variables was carried out in different time
periods. The spatial variability of phytoplankton composition and
biomass of the eastern continental shelf of the Bay of Biscay (north-east
Atlantic Ocean) was assessed using mapping of selected parameters at
both horizontal and vertical scale and combination with remote sensing
data (Lampert et al., 2002). Kriging and IDW interpolation methods
were applied to study coastal marine eutrophication in the Island of
Rhodes, Greece based on the spatial distribution of nutrients and
phytoplankton cell number (Kitsiou et al., 2002) and a number of
ecological indices (Kitsiou and Karydis, 2000). In Cinnirella et al. (2005)
the spatial distribution and uncertainty of groundwater nitrate
concentrations in the Po catchment in Italy were assessed based on a
geostatistical approach. Similarly, Lookman et al. (1995) used kriging to
provide maps on regional scale indicating the sensitivity of certain areas
for rapid P saturation and the resulting eutrophication problems. Kovacs
and Honti (2008) presented a GIS-based methodology for estimating
phosphorus emissions at small scale watersheds and assessing the risk
of eutrophication of small water bodies.
Since coastal eutrophication assessment requires the study of
a large number of parameters, the function and dynamics of each
one could lead to different eutrophication trends (Powell et al.,
1989; Valiela, 1995; Xu et al., 2001). Therefore, there is a need for
appropriate methodologies to synthesize the spatial eutrophication
trends represented by various parameters. Kitsiou and Karydis (1998)
used multiple criteria choice methods to synthesize the spatial
distributions of nutrients and phytoplankton cell number. The result
was a coastal eutrophication map where the trophic status of
Saronicos Gulf, Greece was clearly illustrated. Another two procedures
aiming to synthesize the spatial distributions of seven ecological
indices at the same study area using GIS overlay were also presented
by Kitsiou and Karydis (2000). The overlay technique, performed in
the framework of a GIS, allows the synthesis of different map layers in
order to create a new map. Xu et al. (2001) used also the GIS overlay
technique to synthesize the information from six map layers,
representing the spatial distributions of six chemical, physical and
biological indicators related to eutrophication.
12. Modeling
In coastal eutrophication studies, models have been developed
to explore the relationships between the causes and the effects, to
understand and simulate the physical, bio-geo-chemical and biological
processes and their interactions, and to predict the response of a coastal
ecosystem to forcing related to both physical and anthropogenic origins
(Table 3). Therefore, models provide the means for forecasting the
trends in a coastal area, evaluating management alternatives and
supporting the decision-makers to undertake initiatives.
‘Dynamic’ and ‘Statistical’ models are the two basic types of
mathematical models developed for eutrophication modeling (Rast
et al., 1983). Dynamic models consist of a series of interrelated
differential equations aiming to describe the biological, chemical, and
physical interactions related to aquatic plant growth. The calibration
is carried out for a given water body, therefore these models are
not widely applicable to water bodies of different characteristics.
Statistical or empirical eutrophication models, such as regression
analysis, quantify cause-effect relationships without accounting for
every component involved in the eutrophication process. Models of
this category have been developed by Vollenweider (1969, 1976),
Dillon and Rigler (1974), Jones and Lee (1982) and many others. The
U.S. OECD eutrophication modeling approach was initiated to define
quantifiable relationships between nutrient loads and responses of
water bodies related to eutrophication, aiming to assess and control
eutrophication in lakes and impoundments. In the framework of
792 D. Kitsiou, M. Karydis / Environment International 37 (2011) 778–801
this program, Vollenweider (1969, 1976) developed empirical
relationships between annual total phosphorus loads and annual
average chlorophyll concentrations for a number of European lakes
adjusted for differences in lake morphometry and hydraulic residence
time (Cloern, 2001). Following his valuable approach that formed the
background for future research, other researchers improved and
applied the U.S. OECD load-response regressions to a variety of water
bodies regarding their geographic, morphologic and hydrologic
characteristics (Rast et al., 1983; Golterman, 1991). As already
mentioned these modeling approaches are focused on lakes; therefore,
further analysis would be beyond the objectives of this paper.
Since coastal water bodies vary greatly as far as their response to
nutrient loads is concerned (Tett et al., 2003), it seems unrealistic to
create a single model that will address successfully all the interactions
and variability in coastal areas. It seems more realistic to assess how
a number of factors represented by selected variables affect the response
of a coastal area. The latter is proved by the wide number of partial
modeling approaches found in the literature. For example, Le Gall et al.
(2000) focused on phytoplankton dynamics, Alvera-Azcarate et al.
(2003) on the role of intertidal seaweeds in mesotidal and macrotidal
estuaries, Flipo et al. (2007) on modeling nitrate fluxes at the catchment
scale. Nijboer and Verdonschot (2004) stated that the most important
variables for eutrophication modeling should be extracted after a
thorough study of the natural and eutrophication processes in coastal
areas. Scheffer et al. (2003) developed a minimum model with two
ordinary differential equations for assessing regime shifts in shallow
aquatic ecosystems. In addition, Zaldívar et al. (2009) proposed a
modeling approach to analyze regime shifts of primary production in
shallow coastal ecosystems and to identify possible nutrient thresholds
causing shifts between alternative stable states. The approach is based
on previous existing and validated models developed for Mediterranean
coastal lagoons in order to allow the analysis of different scenarios for
ecosystems subjected to strong anthropogenic pressures. The applica-
bility of the models to other regions than those they were developed for
is also an important factor, since the geomorphological characteristics of
coastal areas can affect to a certain degree some mechanisms related to
eutrophication (Becher et al., 2000). The National Academy of Sciences
(2003) suggests the classification of eutrophication models in the
following categories:
(i) The Screening models are simple modeling schemes representing
simplified estimates by combining a range of factors for assessing
eutrophication effects. They can be used to screen sites for actual
or potential eutrophication by predicting the value of an easy
observed variable such as phytoplankton chlorophyll (Tett et al.,
2003).
(ii) The Steady state and tidally averaged models are the simplest
models available that are capable of describing the relationship
between nutrient loads and some of their impact on coastal
ecosystems related to eutrophication process.
(iii) The Dynamic simulation models of one or more dimensions are
more complex approaches and simulate variations in tidal
height and velocity throughout each tidal cycle enabling the
assessment of phenomena varying rapidly within each tidal
cycle.
The LOICZ approach further described in Section 13 includes the
development of horizontal and, to a lesser extent, vertical material
flux information and models across continental basins. Modeling
approaches have been developed for evaluating biogeochemical
processes for C, N and P in the coastal zone (Smith, 2002); a major
target is to determine the relative poise of the coastal zone with
regard to net carbon flux based on whether the coastal zone is an
autotrophic or a heterotrophic global compartment (Holligan and
Reiners, 1991). The LOICZ biogeochemical model (LBM) is based on
the mass balance of water and materials (Crossland et al., 2005).
Water and salt are assumed not to undergo significant biogeochemical
transformations within the system, while nutrients behave as non-
conservative compounds due to biogeochemical processing within
the system (Giordani et al., 2008). The theoretical bases and
assumptions of the LOICZ nutrient budget modeling are thoroughly
discussed by Gordon et al. (1995).
Koelmans et al. (2001) stated that though a number of complex
models exist following some typical processes, they differ in their
level of detail describing the process of eutrophication. Furthermore,
they argued on the limitations of integrated models, concerning their
degree of integration and their capability of performing efficiently at a
variety of conditions.
In literature, various modeling approaches ranging from simple to
more complex, of one or multi-dimensional character (Chau, 2004)
are proposed to describe eutrophication dynamics (Lessin et al., 2009;
Soetaert and Middelburg, 2009), but a more detailed description is
beyond the scope of the current review.
13. The need for an integrated approach
Recent studies on coastal eutrophication emphasized its global
dimension and the connections with other global environmental
pressures. Duarte (2009) stated that nowadays a proper assessment of
eutrophication should consider this phenomenon as a component of
global change regarding both its causes and consequences. Therefore,
the selection of appropriate methodologies to assess and manage
eutrophication should take into account the interactions with various
components such as climate change (Lloret et al., 2008), overfishing,
habitat loss and inputs of toxic contaminants. In Table 4 integrated
approaches used for the quantitative assessment of eutrophication
with their objectives, advantages and shortcomings in related studies
are presented.
Nixon (2009) focused on the need to examine eutrophication at
a scale larger than the individual ecosystem in order to include
the majority of the forces that lead to this problem. In 2001, Cloern in
his description of the Phase III conceptual model of the coastal
eutrophication problem stated that eutrophication merits sustained
programs of integrated research and monitoring, since the damage
of coastal regions becomes rapidly pervasive and must be effectively
faced.
Research efforts should not focus only to the understanding of
the environmental and ecosystem processes, but also incorporate
the social and anthropogenic pressures. Diaz and Rosenberg (2008)
argued that the anthropogenic fertilization of marine systems by
excess of nitrogen can lead to a similar ecosystem response such as
coastal upwelling.
Anthropogenic activities carried out in the coastline are directly
related to eutrophication problems, since they represent the social
structure and social dynamics of the area (Nixon, 1995). Therefore,
coastal eutrophication should be examined in a broader context
including also socio-economic aspects. As reported by Karydis (2001)
in a short review on quantitative methodology, the problem of
eutrophication apart from being identified and assessed as such
should also be co-evaluated with socio-economic variables. The latter
is of major importance since decision-makers adopt measures to
protect the environmental quality of coastal areas based on both the
scientists' proposal and the public opinion.
The evolution of the first conceptual model of eutrophication
(Cloern, 2001) led to a more integrated approach with an explicit
recognition of the direct and indirect responses, the consideration
of impacts on the Earth System regarding climate and the human
health and socio-economic costs that influence the sustainability of the
human population. Therefore, the social and economic costs of human
disturbance to the coastal zone should be evaluated. Underdal et al.
(1989) argued that an exceptional bloom of the toxic flagellate
Chrysochromulina polylepsis was responsible for the death of more
than 500 tons of farmed fish valued at US $4.5 million. Similar studies
Table 4
Integrated approaches used for the quantitative assessment of eutrophication. Objectives, advantages and shortcomings in assessing eutrophication are provided.
Integrated approach
DPSIR
Systems of global character: LOICZ,
C-GTOS, GLOBEC, IMBER
MCA and mapping
Spatial analysis and remote sensing
Spatial analysis and mapping
Statistics and remote sensing
Statistics/spatial analysis/mapping
Modeling/remote sensing/mapping
Objectives in eutrophication studies
Evaluate different measures for reducing the
input of nutrients and preventing coastal
eutrophication.
Study of the coastal zone as one system.
Observation, modeling and analysis of
ecosystems related to socio-economic
conditions of coastal populations.
Spatial distribution of eutrophication trends
and relative ranking of study areas.
Synthesis of the spatial distributions of
variables related to eutrophication to produce
a eutrophication thematic map.
Spatial analysis of satellite data sets at large
spatial scale to assess eutrophication trends.
Spatial distribution of eutrophication trends
illustrated on thematic maps.
Synthesis of the spatial distributions of
variables related to eutrophication to produce
a eutrophication thematic map.
Statistical analysis of large data sets.
Development of accurate algorithms to assess
coastal eutrophication trends.
Assessment of the accuracy of spatial analysis
and interpolation methods applied in
eutrophication studies.
Increase the accuracy of forecasting spatial
eutrophication trends.
Explore relationships between causes and
effects of coastal eutrophication.
Development of eutrophication thematic maps
based on a number of inter-related variables.
Advantages Shortcomings References
Uses a core set of indicators considering human Not reported yet. Nunneri and Hofmann (2005)
activities as an integral part of the ecosystem. Zaldívar et al. (2008a)
Forecast the responses of the marine ecosystem Assessment at a global scale is not always EEA (2001)
to global change. Provide a comprehensive representative of processes at local spatial scales. Nunneri and Hofmann (2005)
understanding of ocean responses to global change Restrepo (2008)
D. Kitsiou, M. Karydis / Environment International 37 (2011) 778–801
and the effects on the earth and human society.
Detection of eutrophication trends including The development of a map illustrating the Kitsiou and Karydis (1998)
variables of various origins, i.e. socio-economic synthesis of spatial distributions of variables Gomes and Lins (2002)
criteria. requires characterization of the classes of Zhang and Huang (2011)
Assignment of weights to the spatial distributions eutrophication (i.e. eutrophic, upper mesotrophic,
produced. lower mesotrophic, oligotrophic area).
Use of large data sets than the fragmented Spatial resolution of satellite data should be Eleveld and van der Woerd (2006)
information of in situ data. appropriate related to the scale of the study area. Shevyrnogov and Vysotskaya (2006)
Detection of spatial autocorrelation and anisotropies An optimised sampling design is required to Legendre and Fortin (1989)
in the study area. provide the maximum information about the Kitsiou and Karydis (2000)
system derived from all related variables.
Increase of the accuracy of the derived spatial Requirement of in situ data to be correlated to Kabbara et al. (2008)
distributions of variables. satellite data sets. Gohin et al. (2008)
Development of thematic maps of eutrophication Need for additional in-situ data for the validation Webster and Oliver (2001)
of high accuracy. process. Bello-Pineda and
Hernandez-Stefanoni (2007)
Remote sensing data are used as input in modeling Spatial and temporal resolution of satellite data Fontana et al. (2009)
approaches and/or control data sets for evaluating should be appropriate related to the scale of the Nobre et al. (2005)
the accuracy of the models. study area.
No need for in situ data to develop Accuracy of the maps depends on the accuracy of
eutrophication maps. the model.
793
794 D. Kitsiou, M. Karydis / Environment International 37 (2011) 778–801
can be found in the literature (Chang, 1994; Colwell, 1996). In addition,
questions such as “what are the cumulative economic and social costs
of anthropogenic disturbance to coastal ecosystems, and how can
we quantify those losses on a global scale?” or “How does nutrient
enrichment in concert with other disturbances, cause habitat changes
and impact human health?” should be answered (Cloern, 2001).
A participatory approach has been proposed by Nunneri and
Hofmann (2005) based on the DPSIR (Driver Pressure State Impact
Response) analytical tool to evaluate different measures for reducing
the input of nutrients and preventing eutrophication of coastal waters.
DPSIR uses a core set of indicators for environmental performance,
including eutrophication issues, and considers human activities as an
integral part of the ecosystem. Zaldívar et al. (2008a) gives a detailed
description of the DPSIR framework and its application to eutrophi-
cation in coastal waters (EEA, 2001).
Scientists should understand in depth the complexity of the
processes and the factors involved in the eutrophication phenomenon,
work in a cross-disciplinary basis and convey their outputs to coastal
managers and legislators in a simplified way. In this framework, issues
related to coastal marine eutrophication are considered in a number of
developed systems of global character, such as LOICZ, GOOS, C-GTOS,
GLOBEC and IMBER. The Land–Ocean Interactions in the Coastal Zone
(LOICZ) approach is a core project of the International Geosphere–
Biosphere Programme (IGBP) and the International Human Dimensions
Programme on Global Environmental Change (IHDP) that deals with the
study of global environmental change. LOICZ involves scientists who
investigate changes in the biology, chemistry and physics of the coastal
zone and develop protocols and tools that allow the assessment of site-
specific and global coastal processes (Talaue-McManus et al., 2003). The
main goal and the challenge of LOICZ is to bring together the combined
expertise of natural and social sciences to study the coastal zone as one
system, aiming to assess global perspectives of water and sediment
loads into the coastal zone and the impact of human activities on natural
systems; in other words, to extrapolate from the individual budget sites
to the global coastal zone (Crossland et al., 2005).
Restrepo (2008) used the LOICZ approach to understand the
natural and human-induced factors that have produced the observed
patterns of water discharge and sediment load of the Magdalena River
into the Caribbean Sea and to relate these processes to the impact
on coastal ecosystems. Giordani et al. (2008) applied the LOICZ
biogeochemical model (LBM) that is based on the mass balance of
water and materials (Crossland et al., 2005), at different temporal
Fig. 3. Flow chart showing the interaction of data analysis methods for assessing coastal eutrophication and fields of application.
and spatial scales in 17 Italian lagoons; the results indicated that
the LBM seems to be capable of representing the wide range of trophic
conditions associated with shallow coastal ecosystems.
The Global Ocean Observing System (GOOS) is a permanent global
system for observations, modeling and analysis of marine and ocean
variables to support accurate description of the current state of the
sea and forecasts based on marine environmental conditions and
social impacts. GOOS allows all data to be accessible to the public and
researchers in common simple methods. The Chlorophyll Global
Integrated Network (ChloroGIN) sponsored by GOOS, aims to promote
in situ measurement of chlorophyll in combination with satellite
estimates. The Global Terrestrial Observing System (GTOS) is a
programme for observations, modeling, and analysis of terrestrial
ecosystems to support sustainable development. In recognition of
the importance of coastal ecosystems a Coastal Panel (C-GTOS) was
developed in collaboration with other coastal programmes and interna-
tional initiatives. C-GTOS includes issues related to human dimensions
and habitat alteration, water cycle and water quality. The importance of
human dimension is highlighted by the additional efforts carried out on
the socio-economic conditions of coastal populations in coordination
with GOOS. GLOBEC, a study of Global Ocean Ecosystem Dynamics was
initiated in 1990 and included a number of Regional Programmes and
National Activities “to advance our understanding of the structure and
functioning of the global ocean ecosystem, its major subsystems, and its
response to physical forcing so that a capability can be developed to
forecast the responses of the marine ecosystem to global change”.
The Integrated Marine Biochemistry and Ecosystem Research
(IMBER) project focused to provide a comprehensive understanding
of, and accurate predictive capacity for, ocean responses to accelerating
global change and the consequent effects on the Earth System and
human society.
As mentioned above, the combination of different methods is
considered as a prerequisite to achieve a holistic approach of coastal
eutrophication (Fig. 3). Kitsiou et al. (2002) applied a combination of
spatial analysis and MCA for integrating the eutrophication trends in
the coastal area of Rhodes, Greece using a number of variables related
to the socio-economic status of the area. Ferrarini et al. (2001) followed
an integrated approach based on 25 environmental and socio-economic
indicators to evaluate the environmental quality in a number of
municipalities. An integrated methodology for the assessment of
estuarine trophic status has also been proposed by Bricker et al.
(2003) to rank the estuarine and coastal areas according to their
 D. Kitsiou, M. Karydis / Environment International 37 (2011) 778–801
eutrophication status and to address management options. Another
hybrid method for eutrophication assessment in coastal ecosystems was
based on the integration of field data and screening models, allowing the
application of different nutrient loading scenarios and therefore,
supporting coastal managers to adopt effective initiatives (Nobre
et al., 2005). Bowen et al. (2007) presented an interactive user-friendly,
web-based modeling tool for nitrogen management in estuaries
(NLOAD) which brings together six different models that predict
nitrogen loading to estuaries and two models that estimate nitrogen
concentrations in coastal waters. NLOAD allows users to estimate N
loads from a watershed to a receiving water body and determine
percentage contributions to total N loads from watershed, fertilizer and
atmospheric deposition; apart from researchers among users are
stakeholders, managers and coastal decision-makers.
In Fig. 3 a flow chart showing the interaction of data analysis
methods for assessing coastal eutrophication is shown. The interac-
tion of various methods leads to the detection of eutrophication
trends and regime shifts in coastal areas. The information acquired is
useful in the field of sustainable coastal management leading to the
development of effective coastal policies. In parallel, information
based on the evaluation of coastal water quality supports both coastal
management and the adoption of policies by decision-makers.
In conclusion, holistic methodologies for assessing coastal eutrophi-
cation which is a prerequisite for Integrated Coastal Zone Management
approaches, should involve: (i) a number of appropriate indicators to
measure the sensitivity of ecosystems to anthropogenic or natural
forcing, as well as including socio-economic issues, (ii) selection and
combination of methods suitable for assessing the interactions among
the various parameters considered and (iii) combination and evaluation
of the results of the different applied methodologies and approaches
in order to make valuable conclusions.
14. Discussion
Eutrophication assessment requires the evaluation of a number of
variables related to nutrient concentrations and phytoplankton such as
chlorophyll concentrations and phytoplankton community structure.
All these variables inseparably interact and interrelate with physical
(temperature, water transparency and oxygen concentration) as well as
other chemical and biological variables (heterotrophic populations). A
valid assessment of the trophic status in an area should be accomplished
by the understanding of eutrophication causes, consequences and
current/future trends. It is therefore necessary to know linkages
between system variables and processes. An additional difficulty is to
assess the anthropogenic signal by discriminating between natural and
human induced ecosystem pressures. The whole assessment system is
complex and a good design for the whole work is needed otherwise the
analysis of data may lead to erroneous conclusions. Clearly defined goals
and objectives should be set at the very beginning and the variables to be
measured should be selected in a clear, definite and realistic way for the
particular work. Holistic approaches are very expensive, time consum-
ing as well as demanding on scientific personnel and they should
therefore focus on regions with problems of eutrophication. The spatial
and temporal scale sampling should also be defined. Undersampling
may lead to deficiencies in defining confidence intervals or getting a
clear outcome on existing trends and pressures. On the other hand
oversampling may result in wasting of money or bad allocation of
sampling resources. As spatial heterogeneity of marine communities is a
fundamental characteristic in the marine environment (Legendre,
1993), the development of a sampling design for optimizing site
location is strongly recommended (Legendre et al., 1989).
The set of data derived from a sampling program designed to study
eutrophication should address the following objectives: (a) to assess
the trophic status of the study area (oligotrophic, mesotrophic, or
eutrophic), (b) to identify and quantify eutrophic trends, (c) to
discriminate between natural and human induced eutrophication,
795
(d) to condense the information from voluminous sets of data, (e) to
use historical data in addition to current data as an invaluable source
of information for detecting temporal trends in marine eutrophication
studies and (f) the outcome from the data analysis should be
understandable not only by the scientists specialized in eutrophica-
tion studies but also by all stakeholders that is public, managers and
policy makers.
Although ecological indices and diversity measurement was a field
of interest limited to ecologists, attitudes changed since the 1992 Rio
Earth Summit, when the measurement of diversity became a matter of
public concern and environmental policy (Magurran, 2004). However,
as every ecological index expresses some aspects of the structure of an
ecosystem (Gauch, 1989), only few indices have been found suitable
to express eutrophic trends (Lamb et al., 2009). Reservations on the
applicability of ecological indices have also been expressed by
Routledge (1979). However, the Water Framework Directive (WFD)
encourages the development and use of indices for water quality
studies. Although indices are the “magic bullets” for policy makers,
being useful to define limits in water quality issues (Paerl, 2006), it
seems to be a simplified procedure to characterize the trophic status
of a given water body (McQuatters-Gollop et al., 2009).
Regime shifts are difficult to analyze because they usually involve
multiple causes acting at multiple scales (Peters et al., 2007).
Eutrophication regime shifts can have varying effects on different
components of the marine ecosystem, since they vary in scale as well
as in drivers; therefore, there are implications to detect, predict and
manage regime shifts. Research efforts to predict or manage regime
shifts have focused on thresholds which are the critical levels of key
variables that control them (Carpenter and Lathrop, 2008). Numerical
values of thresholds are not easy to be defined; however, they are
important in order to estimate benefits and costs of alternative
actions, estimate risks, evaluate scenarios for alternative actions and
develop appropriate models for effective ecosystem management.
Hugget (2005) suggested using these thresholds as a conceptual
framework for the development of strategies for sustainable natural
resources management.
Descriptive statistics can be useful in assessing eutrophication as a
number of questions can be addressed: (a) what is the trophic status
at a specific site? (b) what are the trends concerning eutrophication?
and (c) how are eutrophication variables interrelated and to what
extent?
One-dimensional statistical analysis provides a wide spectrum of
statistical tools for assessment studies (Table 1). Frequency distributions
and summary statistics of individual variables have been used and scales
of eutrophication have been proposed. Probabilistic methods have been
developed (Stefanou et al., 2000) but all of them are based on a single
variable. Outliers although seem to be a promising data analysis tool for
detecting eutrophic trends as well as any other form of pollution, it has
not gotten enough attention by the researchers. The reasons may be that
probabilistic methods on detection of outliers do not appear on standard
statistical textbooks. These techniques have not been standardized by
the statisticians and therefore they cannot be used as “cookbook”
techniques. The limited number of applications does not allow any
conclusions to be drawn as far as the potential and the limitations of
these methods. Whenever outliers are referred in statistical methods,
for example in regression analysis, they are treated as “nuisance” and
they are simply rejected from the array of data points. However, as
outlying values can also be detected in multivariate samples, it seems to
be a promising data analysis tool as eutrophication assessment is usually
carried out using a number of variables.
In spite of the popularity of the ANOVA, the contribution of this
method to eutrophication studies is of limited value (Underwood,
1981; Underwood, 2007). Lognormal transformations distort the
physical information of the raw data. There is also pseudo-replication
in most cases as data points from different depths and seasons are
usually grouped together, thus eliminating the value of the ANOVA.
796 D. Kitsiou, M. Karydis / Environment International 37 (2011) 778–801
Efforts to produce simulated data (Ignatiades et al., 1992; Primpas
and Karydis, 2010a) seem to be a promising approach to the non
normality problem. In addition, experimental designs of ANOVA can
be used to fit different sampling processes and research objectives,
as there is no limit to the number of the simulated observations that
can be produced.
As water quality data do not usually meet the requirements for use
of parametric statistics two options appear: (a) data transformation
and (b) use of non-parametric methods. The first approach is not
always feasible as it may be difficult to accept the relevance of a test
which is valid on transformed data but not valid for the raw data
(Sheskin, 2004). On the other hand, transformed data can be less
sensitive in detecting differences due to the transformations (Primpas
and Karydis, 2010a). Non-parametric methods do not require
assumptions on the distribution of the data and they are not distorted
by outliers or missing data. In addition, most non-parametric methods
are effective with small samples (Conover, 1999).
Multi-dimensional procedures have been used extensively in
community ecology in aquatic studies. The most popular is cluster
analysis; however, there is a wide variety of distance/similarity
indices as well as clustering algorithms. This is a problem because the
results are not always comparable, in spite of the robustness of the
method. The advantages of cluster analysis are (a) the ease to apply as
there are standardized procedures (Ignatiades, 2002b) and many
software packages are commercially available (Krebs, 1999), (b) the
method is non-parametric, (c) the results can be easily understood, as
tree diagrams are familiar to everybody and (d) large and complex
sets of data are summarized. However, tests of significance are usually
lacking and the decision for defining clusters lies on researcher's
expertise and acumen. Principal Component Analysis has been
applied in a number of eutrophication studies but mainly as a tool
for preliminary screening of data, reduction of the dimensionality of
large data sets and detection of spatial/temporal trends (Lundberg
et al., 2005; Lundberg et al., 2009); the method assumes normally
distributed variables. The production of new uncorrelated variables is
very important for assessing marine eutrophication trends, since the
initial variables are strongly intercorrelated; however, the method
cannot identify nonlinear relationships between different input
variables. PCA has also shown to be attractive for detecting regime
shifts in marine ecosystems being able to identify coherent patterns of
variability among a number of time series (Mantua, 2004; Andersen
et al., 2008). The presence of thresholds in the reduced data set
could become more evident to visual inspection; however, further
processing and statistical testing are required. The conclusions drawn
from PCA regarding the identification of regime shifts can be
strengthened by combination with the results of multivariate time
series analysis such as chronological clustering (Andersen et al.,
2008). However, MacFarlane et al. (2000) argued that the Average
Standard Deviates (ASD) method is more appropriate than PCA for
examining regime shifts in fishery production.
MCA methods seem to be effective in assessing coastal eutrophi-
cation trends and they are often included in coastal management
approaches (Fig. 3). Their main advantage is the ability to co-estimate
information of different origin and to assign weights to the variables
considered. However, different MCA methods can produce a different
result when applied to the same decision problem (Gershon and
Duckstein, 1983; Raju et al., 2000). Another criticism of MCA is its
subjective nature, which is mainly apparent during the weighting
procedure. The weights assigned to the criteria are the outcome of
both the choice of the weighting method and the judgement of the
applicant of the method. The optimal choice of the weighting method
could help to minimize the weighted bias; although it is not clear
which weighting technique is least biased (Balasubramaniam et al.,
2007). An evaluation of multiple criteria analysis techniques for water
resource management (Hajkowicz and Higgins, 2008) suggested that
in spite of the fact that the selection of a MCA method is important,
more emphasis should be given on the initial structuring of the
decision problem. MCA methods are distribution-free, which means
that they do not require any assumptions for the data or dependence
on parametric procedures and therefore, integration of any type of
information can be handled; the latter is quite important due to the
multi-dimensional nature of coastal marine eutrophication. Another
advantage of MCA is the possibility to be integrated and performed in
the framework of a GIS (Gomes and Lins, 2002) providing a flexible
environment for the assessment of coastal eutrophication issues at
spatial scale. Zhang and Huang (2011) implemented a spatial MCA in
a GIS environment to evaluate nitrogen loss potential at a basin level.
The produced maps of nitrogen loss potential proved useful means for
the decision-making process of non-point source pollution
management.
Spatial analysis and mapping techniques are widely applied in
coastal eutrophication studies (Table 4), since they provide the means
for acquiring a clear view of the spatial structure and heterogeneity
of the related variables and an illustration of their spatial distributions
in a map format. The spatial distributions developed are based on
appropriate interpolation methods and their accuracy depends on (i)
the initial data set originated from sampling surveys, (ii) the selected
interpolation method and (iii) the effectiveness of the application of
the method. The development of a sampling design should provide
the maximum information about the system examined. However, the
collection of observations from a large number of points in the study
area without setting specific objectives and the prerequisites of the
methodologies to be applied, does not guarantee the acquirement of
valuable data sets and therefore, the extraction of accurate conclu-
sions (Frontier, 1983). Therefore, when spatial analysis methods and
especially interpolation methods are applied, information should be
collected from an optimum number of sampling sites located at
optimum positions; the extent of the study area, previous knowledge
of the ecosystem and the spatial behavior of the variables under study
should be carefully considered. MacEachren and Davidson (1987)
argued that data measurement accuracy, data density, data distribu-
tion, and spatial variability have the greatest influence on interpola-
tion accuracy. Furthermore, a greater number of replicates from only
the optimum sampling sites could be easier afforded and analyzed
in future surveys, providing valuable time series for estimating
the system variability at spatio-temporal scale. The latter is of great
importance in coastal eutrophication assessment, and therefore
application of spatio-temporal interpolation methods (Li and Revesz,
2004) in this field could be an incentive to develop more effective
integrated approaches.
The selection of the appropriate interpolation method is another
important factor in mapping accuracy. The performance of interpo-
lation methods has been studied in terms of the accuracy of estimates,
when they are applied to data sets collected from coastal areas. The
performance of the methods has been mainly assessed by comparing
the deviations of estimates from the measured data through the use of
cross-validation (Webster and Oliver, 2001) and the calculation of
specific statistics (Bello-Pineda and Hernandez-Stefanoni, 2007). The
general conclusion derived from a number of studies (Nalder and
Wein, 1998; Hernandez-Stefanoni and Ponce-Hernandez, 2006) was
that kriging is a more accurate interpolator; however, the Inverse
Distance Weighted methods have the advantage of relative simplicity
and ease of processing. Nevertheless, since kriging requires initially
the application of variogram analysis, the accuracy of the results is
achieved only if the number of observations is large enough and if a
careful selection of the models of semi-variograms is carried out
(Kravchenko and Bullock, 1999).
Spatial distributions of eutrophication variables can be also the
output from the processing of satellite data (Table 4). Satellite data
are very useful when estimation of the trophic status of coastal areas and
analysis of the observed trends are required, especially at large spatial
scales. However, they are not always effective unless they are combined
 D. Kitsiou, M. Karydis / Environment International 37 (2011) 778–801
with in-situ measurements carried out by oceanographic vessels in
order to develop accurate algorithms to calculate the concentrations of
the variables under study. Remote sensing cannot substitute classical
oceanographic methods due to a number of reasons. An important
reason is that electromagnetic radiation is very poor at penetrating
water; therefore, remote sensing can only operate on the sea surface
skin. Another limitation is that optical techniques from space platforms
are hampered by clouds and the limited temporal resolution of the
satellite imagery. The latter prevent the use of these data sets to create
long time series; therefore, they are very often associated to models or/
and combined to satellite data acquired from other sensors. In addition,
during eutrophication assessment at low spatial scales, such as bays of
limited geographical extent, there is a lack of satellite data of very high
spatial resolution; therefore, most of the times additional in situ
measurements are required.
The selection of the satellite data sets for assessing eutrophication
in a coastal area should be based on: (i) the specific characteristics
of the satellite sensor i.e. spectral, spatial and temporal resolution,
(ii) the morphological characteristics of the study area, and (iii) the
spatial scale. In many coastal eutrophication assessments satellite
data are used in combination with other methodologies; they are
used as input in modeling approaches or as control data sets for the
evaluation of the accuracy of other methodologies. Satellite data can
also be incorporated in GIS databases and analyzed in relation to data
of different origin.
The need for eutrophication modeling of coastal systems has been
highlighted by the increased pressure on coastal ecosystems (Ferreira
et al., 2007). Boynton et al. (1996) argued that it is possible to develop
Vollenweider's type models for some coastal lagoons and estuaries;
however these models are significantly different from the lake models.
In addition, Borum (1996) showed that for 51 estuaries studied; only
36% of the variance of phytoplankton primary production was
correlated with the N-loading rate. Therefore, the Phase I conceptual
model might not apply in estuaries (Cloern, 2001). Though modeling
approaches constitute valuable tools in coastal eutrophication assess-
ment, their application involves substantial uncertainty due to both
model structure and variables (Arhonditsis et al., 2007). In addition,
models are considered as simplifications of reality and do not usually
include all the parameters involved in the eutrophication process,
focusing on partial aspects of the phenomenon. Furthermore,
calibration of models is carried out using specific data sets of variables
representative of a specific location. Update of these data sets requires
recalibration of the model. On the other hand, it is not evident that the
same model could be immediately applicable in another region
without re-calibration and collection of additional data related to the
particular characteristics of the new study area (Fontana et al., 2009).
Another discussion about models refers to the degree of their
complexity. As Ferreira et al. (2007) stated the challenge is to cross-
validate and improve simple models and apply complex modeling to
fill data gaps and explore specific scenarios. The latter constitutes a
useful tool in forecasting the response of coastal ecosystems to specific
changes or pressures. Models can be developed, incorporated and run
in a GIS environment and be combined with spatial analysis methods
and mapping techniques; tools of high integrity for assessing coastal
marine eutrophication issues can become therefore available. In
addition, according to Cloern (2001) the challenge is to integrate
mathematical representations of benthic and pelagic systems with
climate, watershed, atmosphere and economic models.
The development of methods that provide early warning of
eutrophication regime shifts is considered as an important scientific
challenge. A promising research path aims to combine empirical studies
of coastal marine ecosystems with theoretical and modeling studies
of other systems for which the dynamics are better understood. The
ability to manage ecosystems to avoid regime shifts would be improved
by predicting how close an ecosystem is to critical thresholds (Gordon
et al., 2008).
797
The Water Framework Directive (2000/60/EC) and other recent EC
legislation claimed the need for developing tools capable of classifying
water bodies according to their quality and applicable to different
water body types. Therefore, integrated approaches for combining,
analyzing and evaluating information from various interrelated
variables are important to manage coastal eutrophication and guide
action plans (Fig. 3). In general, the ability to monitor and model
coastal marine ecosystems is improving, since new global observation
tools are available, such as the GOOS. These large data sets are of
limited value without a deep understanding of coastal processes;
however, cooperative, multidisciplinary studies such as GLOBEC and
IMBER help to fill the gaps of our knowledge about ecosystem
functions. Artioli et al. (2008) evaluated the effectiveness of recently
adopted policies to reduce anthropogenic nutrient inputs to European
Seas. Their aim was to assess and to compare changes in the nutrient
budgets (N and P) of four sub-regional basins. The results highlighted
the importance of the regional differences in the effectiveness of the
reduction policies. It is argued that the ‘one shoe fits all’ approach to
coastal marine eutrophication issues is inappropriate. Consequently,
requirement of different targets is needed at regional scale with
subsidiary targets for individual sea basins.
Acknowledgment
The authors would like to thank the anonymous reviewers for their
constructive comments on the manuscript.
References
Aguilera PA, Castro H, Rescia A, Schmitz MF. Methodological development of an index
of coastal water quality: application in a tourist area. Environ Manage 2001;27(2):
295–301.
Almasri MN, Kaluarachchi JJ. Multi-criteria decision analysis for the optimal
management of nitrate contamination of aquifers. J Environ Manage 2005;74:
365–81.
Alvera-Azcarate A, Ferreira JG, Nunes JP. Modelling eutrophication in mesotidal and
macrotidal estuaries. The role of intertidal seaweeds. Estuar Coast Shelf S 2003;57:
715–24.
Ananda J, Herath G. A critical review of multi-criteria decision making methods with
special reference to forest management and planning. Ecol Econ 2009;68:2535–48.
Andersen JH, Schluter L, AErtebjerg G. Coastal eutrophication: recent developments in
definitions and implications for monitoring strategies. J Plankton Res 2006a;28:
621–8.
Andersen T, Carstensen J, Zaldívar JM. Literature database on statistical methods for
threshold identification. THRESHOLDS: Thresholds of Environmental Sustainability,
D2.2.1, Sixth Framework Programme; 2006b. http://www.thresholds-eu.org.
Andersen T, Carstensen J, Hernández-García E, Duarte CM. Ecological thresholds and
regime shifts: approaches to identification. Trends Ecol Evol 2008;24(1):49–57.
Anttila S, Kairesalo T, Pellikka P. A feasible method to assess inaccuracy caused by
patchiness in water quality monitoring. Environ Monit Assess 2008;142:11–22.
Arhonditsis GB, Qian SS, Stow CA, Lamon EC, Reckhow KH. Eutrophication risk
assessment using Bayesian calibration of process-based models: application to a
mesotrophic lake. Ecol Model 2007;208:215–29.
Artioli Y, Friedrich J, Gilbert AJ, et al. Nutrient budgets for European seas: a measure
of the effectiveness of nutrient reduction policies. Mar Pollut Bull 2008;56(9):
1609–17.
Baan PJA, van Buuren JT. Testing of indicators for the marine and coastal environment in
Europe. Part 3: Present state and development of indicators for eutrophication,
hazardous substances, oil and ecological quality. European Environment Agency,
Copenhagen. Technical Report No. 86; 2003.
Balasubramaniam A, Boyle AR, Voulvoulis N. Improving petroleum contaminated land
remediation decision-making through the MCA weighting process. Chemosphere
2007;66:791–8.
Bald J, Borja A, Muxica I, Franco V, Valencia V. Assessing reference conditions and
physico-chemical status according to the European Water Framework Directive: a
case-study from the Basque Country (Northern Spain). Mar Pollut Bull 2005;50:
1508–22.
Barnett V, Lewis T. Outliers in statistical data. Chichester: John Wiley and Sons; 1994.
Becher KD, Schnoebelen DJ, Akers KKB. Nutrients discharged to the Mississippi River
from eastern Iowa watersheds, 1996–1997. J Am Water Resour As 2000;36:161–73.
Bello-Pineda J, Hernandez-Stefanoni JL. Comparing the performance of two spatial
interpolation methods for creating a digital bathymetric model of the Yucatan
submerged platform. PanamJAS 2007;2(3):247–54.
Bierman P, Lewis M, Ostendorf B, Tanner J. A review of methods for analysing spatial
and temporal patterns in coastal water quality. Ecol Indicat 2011;11:103–114.
Blanchet FG, Legendre P, Borcard D. Modelling directional spatial processes in
ecological data. Ecol Model 2008;215:325–36.
798 D. Kitsiou, M. Karydis / Environment International 37 (2011) 778–801
Boelsch DF. Application of numerical classification in ecological investigations of water
pollution. U.S. Environmental Research Agency, EPA-600/3-77-033; 1977.
Borja A, Dauer DM. Assessing the environmental quality status in estuarine and coastal
systems: comparing methodologies and indices. Ecol Indicat 2008;8:331–7.
Borja A, Franco J, Perez V. A marine biotic index to establish the ecological quality of
soft-bottom benthos within European estuarine and coastal environments. Mar
Pollut Bull 2000;40(12):1100–14.
Borja J, Franco J, Muxica I. Classification tools for marine ecological quality assessment:
the usefulness of macrobenthic communities in an area affected by a submarine
outfall. ICES CM 2003;J02:1-10.
Borum J. Shallow waters and land/sea boundaries. In: Jsrgensen BB, Richardson K, editors.
Eutrophication in coastal marine ecosystems. Washington: American Geophysical
Union; 1996. p. 179–203.
Bowen JL, Ramstack JM, Mazzilli S, Valiela I. NLOAD: an interactive, web-based modeling
tool for nitrogen management in estuaries. Ecol Appl 2007;17(5):S17–30.
Box GEP, Tiao GC. Intervention analysis with applications to economic and
environmental problems. J Am Stat Assoc 1975;70:10–79.
Boynton WR, Hagy JD, Murray L, Stokes C, Kemp WM. A comparative analysis of
eutrophication patterns in a temperate coastal lagoon. Estuaries 1996;19:408–21.
Bricker SB, Ferreira JG, Simas T. An integrated methodology for assessment of estuarine
trophic status. Ecol Model 2003;169:39–60.
Burger J. Bioindicators: a review of their use in the environmental literature 1970–2005.
Environ Bioindicators 2006;1(2):136–44.
Burrough PA, McDonnell RA. Principles of geographic information systems: spatial
information systems and geostatistics. Oxford: Oxford University Press; 2000.
Cambardella CA, Moorman TB, Novak JM, et al. Field-scale variability of soil properties
in Central Iowa soils. Soil Sci Soc Am J 1994;58:1501–11.
Cao Y, Bark AW, Williams WP. A comparison of clustering methods for river benthic
community analysis. Hydrobiologia 1997;347:25–40.
Carlson RE. A trophic state index for lakes. Limnol Oceanogr 1977;22(2):361–9.
Carpenter SR. Regime shifts in Lake ecosystems: pattern and variation. Volume 15 in the
excellence in ecology series. Oldendorf/Luhe, Germany: Ecology Institute; 2003.
Carpenter SR, Lathrop RC. Probabilistic estimate of a threshold for eutrophication.
Ecosystems 2008;11:601–13.
Chang FH. New Zealand: major shellfish poisoning (NSP) in early '93, Intergov
Oceanogr Comm UNESCO. Harmful Algal News 1994;8:1–2.
Chau KW. A three-dimensional eutrophication modeling in Tolo Harbour. Appl Math
Model 2004;28:849–61.
Chavula G, Brezonik P, Thenkabail P, Johnson T, Bauer M. Estimating chlorophyll
concentration in Lake Malawi from MODIS satellite imagery. Phys Chem Earth Parts
A B C 2009;34(13–16):755–60.
Cinnirella S, Buttafuoco G, Pirrone N. Stochastic analysis to assess the spatial distribution
of groundwater nitrate concentrations in the Po catchment (Italy). Environ Pollut
2005;133:569–80.
Clarke KR. Comparisons of dominance curves. J Exp Mar Biol Ecol 1990;138:143–57.
Clarke KR. Nonparametric multivariate analyses of changes in community structure.
Aust J Ecol 1993;18:117–43.
Cliff AD, Ord JK. Spatial autocorrelation (monographs in spatial and environmental
systems analysis). London: Pion Ltd; 1973.
Cloern JE. Our evolving conceptual model of the coastal eutrophication problem. Mar
Ecol Prog Ser 2001;210:223–53.
Colwell RR. Global climate and infectious disease: the cholera paradigm. Science
1996;274:2025–31.
Conover WJ. Practical nonparametric statistics. John Wiley & Sons; 1999.
Cressie NAC. Statistics for spatial data. New York: Wiley; 1993.
Crossland CJ, Kremer HH, Lindeboom HJ, Crossland JIM, Le Tissier MDA. Coastal fluxes in
the Anthropocene. Berlin: Springer; 2005.
Cruzado A, Velasquez Z, Perez MD, Bahamon N, Grimaldo NS, Ridolfi F. Nutrient fluxes
from the Ebro River and subsequent across-shelf dispersion. Cont Shelf Res
2002;22:349–60.
Danilov RA, Ekelund NGA. Comparative studies on the usefulness of seven ecological
indices for the marine coastal monitoring close to the shore on the Swedish East
coast. Environ Monit Assess 2001;66:265–79.
Day RW, Quinn GP. Comparisons of treatments after an analysis of variance in ecology.
Ecol Monogr 1989;59:433–63.
de Jong F. Marine eutrophication in perspective. Berlin: Springer-Verlag; 2006.
de Jonge VN, Elliott M, Orive E. Causes, historical development, effects and future
challenges of a common environmental problem: eutrophication. Hydrobiologia
2002;475:1-19.
deYoung B, Barange M, Beaugrand G, et al. Regime shifts in marine ecosystems:
detection, prediction and management. Trends Ecol Evol 2008;23(7):402–9.
Diaz RJ, Rosenberg R. Spreading dead zones and consequences for marine ecosystems.
Science 2008;321:926–9.
Digby PGN, Kempton RA. Multivariate analysis of ecological communities. London:
Champan & Hall; 1987.
Dillon PJ, Rigler FH. A test of a simple nutrient budget model predicting the phosphorus
concentration in lake water. J Fish Res Bd Can 1974;31:1771–8.
Draper NR, Smith H. Applied regression analysis (Wiley series in probability and
statistics). USA: John Wiley & Sons Inc.; 1998.
Duarte CM. Coastal eutrophication research: a new awareness. Hydrobiologia 2009;629:
263–9.
Dugdale RC. Nutrient limitation in the sea: dynamics, identification and significance.
Limnol Oceanogr 1967;12:685–95.
Dunteman GH. Principal component analysis. London: Sage Publications; 1989.
Dutilleul P. Spatial heterogeneity and the design of ecological field experiments.
Ecology 1993;74:1646–58.
Ebbesmeyer CC, Cayan DR, McLain DR, Nichols FH, Peterson DH, Redmond KT. 1976 step in
the Pacific climate: forty environmental changes between 1968–1975 and 1977–
1984. In: Betancourt JL, Sharp VL, editors. Proceedings of the Seventh Annual Pacific
Climate (PACLIM) workshop, April 24 1990. California Dept. of Water Resources.
Interagency Ecological Studies Program Technical Report 26.; 1991. p. 115–26.
EC. Council Directive 91/271/EEC of 21 May 1991 concerning urban waste-water
treatment. OJ L135; 30.5; 1991a.
EC. Council Directive concerning the protection of waters against pollution caused by
nitrates from agricultural sources (91/676/EEC). Off J Eur Commun L375(1–8);
31.12; 1991b.
EC. European Commission Directive 2000/60/EC of the European Parliament and of the
Council of 23 October 2000 establishing a framework for community action in the
field of water policy. Brussels Off J Eur Commun 2000;L327.
EEA. Eutrophication in Europe's coastal waters. Topic report no. 7. Copenhagen: European
Environmental Agency; 2001.
EEA. Nutrients in European ecosytems. Environmental assessment report no. 4.
Copenhagen: European Environmental Agency; 1999.
Eleveld MA, van der Woerd HJ. Patterns in water quality products of the North Sea:
variogram analyses of single and compound SeaWiFS CHL & SPM grids. In: Kerle N,
Skidmore AK, editors. Remote sensing: from pixels to processes. The Netherlands:
Ensche, ISPRS Proceedings Technical Commission, vol. VII. ; 2006.
Elliot M. The analysis of macrobenthic community data. Mar Pollut Bull 1994;28(2):
62–4.
Estrada M, Marrase C, Latasa M, Berdalet E, Delgado M, Riera T. Variability of deep
chlorophyll maximum characteristics in the Northwestern Mediterranean. Mar
Ecol Prog Ser 1993;92:289–300.
Everitt BS. A Monte-Carlo investigation of the Likelihood Ratio Test for the number of
components in a mixture of normal distributions. Multivar Behav Res 1981;16(2):
171–80.
Everitt BS, Landau S, Leese M. Cluster analysis. London: Arnold; 2001.
Ferrarini A, Bodini A, Becchi M. Environmental quality and sustainability in the province
of Reggio Emilia (Italy): using multi-criteria analysis to assess and compare
municipal performance. J Environ Manage 2001;63:117–31.
Ferreira JG, Bricker SB, Simas TC. Application and sensitivity testing of a eutrophication
assessment method on coastal systems in the United States and European Union.
J Environ Manage 2007;82:433–45.
Ferris R, Humphrey JW. A review of potential biodiversity indicators for application in
British Forests. Forestry 1999;72(4):313–28.
Field JG, Clarke KR, Warwick RM. A practical strategy for analyzing multispecies
distribution patterns. Mar Ecol Prog Ser 1982;8:37–52.
Flipo N, Jeannee N, Poulin M, Even S, Ledoux E. Assessment of nitrate pollution in the
Grand Morin aquifers (France): combined use of geostatistics and physically based
modeling. Environ Pollut 2007;146:241–56.
Fontana C, Grenz C, Pinazo C, Marsaleix P, Diaz F. Assimilation of SeaWiFS chlorophyll
data into a 3D-coupled physical–biogeochemical model applied to a freshwater-
influenced coastal zone. Cont Shelf Res 2009;29:1397–409.
Fowler J, Cohen L, Jarvis P. Practical statistics for field biology. Chichester: John Wiley &
Sons; 1998.
Frontier S. Stratégies d'échantillonnage en écologie. Québec: Masson, Presses de
l'Université Laval; 1983.
Garcia CAE, Garcia VMT, McClain CR. Evaluation of SeaWiFS chlorophyll algorithms in
the Southwestern Atlantic and Southern Oceans. Remote Sens Environ 2005;95:
125–37.
Gauch HG. Multivariate analysis in community ecology. Cambridge: Cambridge University
Press; 1989.
Georgopoulos PG, Seinfeld JH. Statistical distributions of air pollutant concentrations.
Environ Sci Technol 1982;16:A401–16.
Gershon M, Duckstein L. Multiobjective approaches to river basin planning. J Water Res
Pl Manage Asce 1983;109:13–28.
Giordani G, Austoni M, Zaldívar JM, Swaney DP, Viaroli P. Modelling ecosystem
functions and properties at different time and spatial scales in shallow coastal
lagoons: an application of the LOICZ biogeochemical model. Estuar Coast Shelf S
2008;77:264–77.
Giordani G, Zaldivar JM, Viaroli P. Simple tools for assessing water quality and trophic
status in transitional water ecosystems. Ecol Indicat 2009;9(5):982–91.
Giovanardi F, Tromellini E. Statistical assessment of trophic conditions: application of
the OECD methodology to the marine environment. In: Vollenweider RA, Marchetti
R, Viviani R, editors. Marine Coastal Eutrophication. London: Elsevier Science
Publications; 1992. p. 211–33.
Gitelson A. Algorithms for remote sensing of phytoplankton pigments in inland waters.
Adv Space Res 1993;13(5):197–201.
Giupponi C, Eiselt B, Ghetti PF. A multicriteria approach for mapping risks of agricultural
pollution for water resources: the Venice Lagoon Watershed case study. J Environ
Manage 1999;56:259–69.
Gohin F, Saulquin B, Oger-Jeanneret H, et al. Towards a better assessment of the
ecological status of coastal waters using satellite-derived chlorophyll-a concentra-
tions. Remote Sens Environ 2008;112:3329–40.
Golterman HL. Reflections on post-OECD eutrophication models. Hydrobiologia
1991;218:167–76.
Gomes EG, Lins MPE. Integrating geographical information systems and multi-criteria
methods: a case study. Ann Oper Res 2002;116:243–69.
Gons HJ, Auer MT, Effler SW. MERIS satellite chlorophyll mapping of oligotrophic and
eutrophic waters in the Laurentian Great Lakes. Remote Sens Environ 2008;112(11):
4098–106.
Gordon Jr DC, Boudreau PR, Mann KH, et al. LOICZ biogeochemical modelling guidelines.
LOICZ report and studies no. 5; 1995.
 D. Kitsiou, M. Karydis / Environment International 37 (2011) 778–801
Gordon LJ, Peterson GD, Bennett EM. Agricultural modifications of hydrological flows
create ecological surprises. Trends Ecol Evol 2008;23(4):211–9.
Gower JC, Legendre P. Metric and Euclidean properties of dissimilarity coefficients.
J Classif 1986;3:5-48.
Gray J. Eutrophication in the sea. In: Colombo G, Viviani R, editors. Marine
eutrophication and pollution dynamics. Fredensborg: Olsen and Olsen; 1992.
Hajdu LJ. Graphical comparison of resemblance measures in phytosociology. Vegetatio
1981;48:47–59.
Hajkowicz S. A comparison of multiple criteria analysis and unaided approaches to
environmental decision making. Environ Sci Policy 2007;10:177–84.
Hajkowicz S, Higgins A. Comparison of multiple criteria analysis techniques for water
resource management. Eur J Oper Res 2008;184:255–65.
Halser AD. Eutrophication of lakes by domestic drainage. Ecology 1947;28(4):383–95.
Hare SR, Mantua NJ. Empirical evidence for North Pacific regime shifts in 1977 and
1989. Prog Oceanogr 2000;47:103–45.
Hartog JA, Hinloopen E, Nijkamp P. A sensitivity analysis of multicriteria choice
methods — an application on the basis of the optimal site selection for a nuclear-
power plant. Energy Econ 1989;11:293–300.
Harvey N, Caton B. Coastal management in Australia. Melbourne: Oxford University
Press; 2003.
Hawkins DM. Identification of outliers. London: Chapman and Hall; 1980.
Heip C. Eutrophication and Zoobenthos dynamics. Ophelia 1995;41:113–36.
HELCOM. The Third Baltic Sea pollution load compilation. Baltic Sea environment
proceedings, no. 70. Helsinki, Finland: Helsinki Commission; 1998.
Hernandez-Stefanoni JL, Ponce-Hernandez R. Mapping the spatial variability of plant
diversity in a tropical forest: comparison of spatial interpolation methods. Environ
Monit Assess 2006;117:307–34.
Herrera-Silveira JA, Morales-Ojeda SM. Evaluation of the health status of a coastal
ecosystem in southeast Mexico: assessment of water quality, phytoplankton and
submerged aquatic vegetation. Mar Pollut Bull 2009;59:72–86.
Heyman U, Ryding SO, Forsberg C. Frequency-distributions of water-quality variables —
relationships between mean and maximum values. Water Res 1984;18:787–94.
Holligan PM, Reiners WA. Predicting the responses of the coastal zone to global change.
Adv Ecol Res 1991;22:211–55.
Howard AF. A critical look at multiple criteria decision making techniques with
reference to forestry applications. Can J For Res 1991;21:1649–59.
Huang B, Jiang B, Li H. An integration of GIS, virtual reality and the Internet for
visualization, analysis and exploration of spatial data. Int J Geogr Inf Sci 2001;15:
439–56.
Hugget AJ. The concept and utility of ‘ecological thresholds’ in biodiversity conservation.
Biol Conserv 2005;124:301–10.
Hutchinson GE. A treatise on limnology. Introduction to lake biology and the
limnoplankton, Volume II. NewYork: John Wiley & Sons; 1967.
Ignatiades L. Photosynthetic capacity at the surface microlayer during the mixing
period. J Plankton Res 1990;12:851–60.
Ignatiades L. The productive and optical status of the oligotrophic waters of the Southern
Aegean Sea (Cretan Sea), Eastern Mediterranean. J Plankton Res 1998;20:985–95.
Ignatiades L. Statistical applications in marine phytoplanktonic studies: part I.
Parametric and non-parametric statistical analyses. In: Subba Rao DV, editor.
Pelagic ecology methodology. Lisse: A.A: Balkema Publishers; 2002a. p. 49–57.
Ignatiades L. Statistical applications in marine phytoplanktonic studies: part II. Analysis
of ecological data. In: Subba Rao DV, editor. Lisse: A.A: Pelagic Ecology Methodology;
2002b.
Ignatiades L, Karydis M. Detection of phytoplankton seasonality trends based on k-
dominance curves. Rapp Comm Int Mer Medit 1990;32:1.
Ignatiades L, Vassiliou A, Karydis M. A comparison of phytoplankton biomass parameters
and their interrelation with nutrients in Saronic Gulf (Greece). Hydrobiologia
1985;128:201–6.
Ignatiades L, Pagou K, Vassiliou A. Long-term response of 6 diatom species to
eutrophication. Oceanol Acta 1986;9:449–56.
Ignatiades L, Karydis M, Pagou K. Patterns of dark 14CO2 incorporation by natural
marine-phytoplankton communities. Microb Ecol 1987;13(3):249–59.
Ignatiades L, Karydis M, Vounatsou P. A possible method for evaluating oligotrophy and
eutrophication based on nutrient concentration scales. Mar Pollut Bull 1992;24:
238–43.
Ignatiades L, Georgopoulos D, Karydis M. Description of the Phytoplanktonic
community of the oligotrophic waters of the SE Aegean Sea (Mediterranean).
Mar Ecol Pubbl Della Stn Zool Di Napoli I 1995;16:13–26.
Isaaks EH, Srivastava RM. An introduction to applied geostatistics. USA: Oxford
University Press; 1989.
Istvanovics V, Osztoics A, Honti M. Dynamics and ecological significance of daily internal
load of phosphorus in shallow Lake Balaton, Hungary. Freshw Biol 2004;49(3):
232–52.
Iverson RL, Esaias WE, Turpie K. Ocean annual phytoplankton carbon and new
production, and annual export production estimated with empirical equations and
CZCS data. Glob Change Biol 2000;6:57–72.
Jaccard J, Becker MA, Wood G. Pairwise multiple comparison procedures — a review.
Psychol Bull 1984;96:589–96.
Jankowski P. Towards participatory geographic information systems for community-
based environmental decision making. J Environ Manage 2009;90:1966–71.
Janssen R. Multiobjective decision support for environmental management. Amsterdam:
Kluwer; 1992.
Janssen R. On the use of multi-criteria analysis in environmental impact assessment in
The Netherlands. J MultiCriteria Decis Anal 2001;10:101–9.
Jones RA, Lee GF. Recent advances in assessing impact of phosphorus loads on
eutrophication-related water quality. J Water Res 1982;16:503–15.
799
Kabbara N, Benkhelil J, Awad M, Barale V. Monitoring water quality in the coastal area of
Tripoli (Lebanon) using high-resolution satellite data. ISPRS J Photogramm Remote
Sens 2008;63:488–95.
Karydis M. Scaling methods in assessing environmental quality — a methodological
approach to eutrophication. Environ Monit Assess 1992;22:123–36.
Karydis M. Environmental quality assessment based on the analysis of extreme values —
a practical approach for evaluating eutrophication. J Environ Sci Heal A Environ Sci
Eng Tox Hazard Subst Control 1994;29:775–91.
Karydis M. Quantitative assessment of eutrophication: a scoring system for character-
ising water quality in coastal marine ecosystems. Environ Monit Assess 1996;41:
233–46.
Karydis M. Assessing levels of eutrophication: a short review on quantitative
methodology. Biol Gallo hellenica 2001;27:135–44.
Karydis M. Eutrophication assessment of coastal waters based on indicators: a literature
review. Glob Nest J 2009;11:373–90.
Karydis M, Ignatiades L. The significance of outlying P–PO4 values in eutrophication
studies. Rapp Comm Int Mer Medit 1992;33:73.
Karydis M, Tsirtsis G. Ecological indices: a biometric approach for assessing
eutrophication levels in the marine environment. Sci Total Environ 1996;186:
209–19.
Kirchner WB, Dillon PJ. An empirical method of estimating the retention of phosphorus
in lakes. Water Resour Res 1975;11(1):182–3.
Kitsiou D, Karydis M. Development of categorical mapping for quantitative assessment
of eutrophication. J Coast Conserv 1998;4:35–44.
Kitsiou D, Karydis M. Categorical mapping of marine eutrophication based on ecological
indices. Sci Total Environ 2000;255:113–27.
Kitsiou D, Tsirtsis G, Karydis M. Developing an optimal sampling design. A case study in
a coastal marine ecosystem. Environ Monit Assess 2001;71:1-12.
Kitsiou D, Coccossis H, Karydis M. Multi-dimensional evaluation and ranking of coastal
areas using GIS and multiple criteria choice methods. Sci Total Environ 2002;284:
1-17.
Koelmans AA, Van der Heijde A, Knijff LM, Aalderink RH. Integrated modelling of
eutrophication and organic contaminant fate & effects in aquatic ecosystems.
review Water Res 2001;35:3517–36.
Koo BK, O'Connell PE. An integrated modelling and multicriteria analysis approach to
managing nitrate diffuse pollution: 1, Framework and methodology. Sci Total
Environ 2006;359:1-16.
Kovacs A, Honti M. Estimation of diffuse phosphorus emissions at small catchment scale
by GIS-based pollution potential analysis. Desalination 2008;226:72–80.
Kravchenko A, Bullock DG. A comparative study of interpolation methods for mapping
soil properties. Agron J 1999;91:393–400.
Krebs CJ. Ecological methodology. Addison Wesley Longman Publ; 1999.
Krom MD, Brenner S, Kress N, Gordon LI. Phosphorus limitation of primary productivity
in the E. Mediterranean Sea. Limnol Oceanogr 1991;36(3):424–32.
Krom MD, Emeis KS, Van Cappelen P. Why is the Eastern Mediterranean phosphorus
limited? Prog Oceanogr 2010;85:236–44.
Lam NSN. Spatial interpolation methods: a review. Am Cartographer 1983;10(2):
129–49.
Lamb EG, Bayne E, Holloway G, et al. Indices for monitoring biodiversity change: are
some more effective than others? Ecol Indicat 2009;9(3):432–44.
Lambshead PJD, Platt HM, Shaw KM. The detection of differences among assemblages of
marine benthic species based on an assessment of dominance and diversity. J Nat
Hist 1983;17(6):859–74.
Lampert L, Queguiner B, Labasque T, Pichon A, Lebreton N. Spatial variability of
phytoplankton composition and biomass on the eastern continental shelf of the Bay
of Biscay (north-east Atlantic Ocean). Evidence for a bloom of Emiliania huxleyi
(Prymnesiophyceae) in spring 1998. Cont Shelf Res 2002;22:1225–47.
Lancaster P, Salkauskas K. Curve and surface fitting: an introduction. London: Academic
Press; 1986.
Le Gall AC, Hydes DJ, Kelly-Gerreyn BA, Slinn DJ. Development of a 2D horizontal
biogeochemical model for the Irish Sea DYMONIS. ICES J Mar Sci 2000;57:1050–9.
Legendre P. Spatial autocorrelation-trouble or new paradigm. Ecology 1993;74(6):
1659–73.
Legendre P, Fortin MJ. Spatial pattern and ecological analysis. Vegetatio 1989;80:
107–38.
Legendre P, Legendre L. Numerical ecology-developments in environmental modelling.
2nd English edition. Elsevier; 2003.
Legendre P, Troussellier M, Jarry V, Fortin MJ. Design for simultaneous sampling of
ecological variables: from concepts to numerical solutions. Oikos 1989;55:30–42.
Lessin G, Ossipova V, Lips I, Raudsepp U. Identification of the coastal zone of the central
and eastern Gulf of Finland by numerical modeling, measurements, and remote
sensing of chlorophyll a. Hydrobiologia 2009;629:187–98.
Li L, Revesz P. Interpolation methods for spatio-temporal geographic data. Comput
Environ Urban Syst 2004;28:201–27.
Li HB, Reynolds JF. A simulation experiment to quantify spatial heterogeneity in
categorical maps. Ecology 1994;75:2446–55.
Linkov I, Satterstrom FK, Kiker G, et al. Multicriteria decision analysis: a comprehensive
decision approach for management of contaminated sediments. Risk Anal 2006;26:
61–78.
Lloret J, Marin A, Marin-Guirao L. Is coastal lagoon eutrophication likely to be
aggravated by global climate change? Estuar Coast Shelf S 2008;78:403–12.
Lookman R, Vandeweert N, Merckx R, Vlassak K. Geostatistical assessment of the
regional distribution of phosphate sorption capacity parameters (Fe–Ox and Al–
Ox) in northern Belgium. Geoderma 1995;66:285–96.
Ludwig JA, Reynolds JF. Statistical ecology: a primer on methods and computing. New
York: John Wiley & Sons; 1988.
800 D. Kitsiou, M. Karydis / Environment International 37 (2011) 778–801
Lundberg C, Lonnroth M, von Numers M, Bonsdorff E. A multivariate assessment of
coastal eutrophication. Examples from the Gulf of Finland, northern Baltic Sea. Mar
Pollut Bull 2005;50:1185–96.
Lundberg C, Jakobsson BM, Bonsdorff E. The spreading of eutrophication in the eastern
coast of the Gulf of Bothnia, northern Baltic Sea — an analysis in time and space.
Estuar Coast Shelf S 2009;82:152–60.
Mabit L, Bernard C. Assessment of spatial distribution of fallout radionuclides through
geostatistics concept. J Environ Radioactiv 2007;97:206–19.
MacEachren AM, Davidson JV. Sampling and isometric mapping of continuous
geographic surfaces. Am Cartographer 1987;14:299–320.
MacFarlane GA, King JR, Beamish RJ. Have there been recent changes in climate? Ask the
fish. Prog Oceanogr 2000;47:147–69.
Magurran AE. Measuring biological diversity. Blackwell Science Ltd; 2004.
Malczewski J. GIS-based multicriteria decision analysis: a survey of the literature. Int J
Geogr Inf Sci 2006;20:703–26.
Manly BFJ. Statistics for environmental science and management. USA: Chapman &
Hall/CRC; 2001.
Mantua N. Methods for detecting regime shifts in large marine ecosystems: a review
with approaches applied to North Pacific data. Prog Oceanogr 2004;60:165–82.
MAP. Municipal wastewater treatment plants in Mediterranean coastal cities. MAP
technical reports, series no. 109; 2008.
Maritorena S, Siegel DA. Consistent merging of satellite ocean color data sets using a
bio-optical model. Remote Sens Environ 2005;94:429–40.
Mason RL, Gunst RF, Hess JL. Statistical design and analysis of experiments. New York:
J. Wiley & Sons Inc.; 1989.
Matheron G. Principles of geostatistics. Econ Geol 1963;58:1246–66.
McIntire CD. The distribution of estuarine diatoms along environmental gradients:
a canonical correlation. Estuar Coast Mar Sci 1978;6(5):447–57.
McQuatters-Gollop A, Gilbert AJ, Mee LD, et al. How well do ecosystem indicators
communicate the effects of anthropogenic eutrophication? Estuar Coast Shelf S
2009;82:583–96.
McQuoid MR, Hobson LA. A 91-year record of seasonal and interannual variability of
diatoms from laminated sediments in Saanich Inlet, British Columbia. J Plankton
Res 1997;19:173–94.
Michelakaki M, Kitsiou D. Estimation of anisotropies in chlorophyll a spatial distributions
based on satellite data and variography. Glob NEST J 2005;7(2):204–11.
Miller PI, Shutler JD, Moore GF, Groom SB. SeaWiFS discrimination of harmful algal
bloom evolution. Int J Remote Sens 2006;27:2287–301.
Moncheva S, Gotsis-Skretas O, Pagou K, Krastev A. Phytoplankton blooms in Black Sea
and Mediterranean coastal ecosystems subjected to anthropogenic eutrophication:
similarities and differences. Estuar Coast Shelf S 2001;53(3):281–95.
Moriki A, Karydis M. Application of multicriteria choice methods in assessing
eutrophication. Environ Monit Assess 1994;33:1-18.
Mumby PJ, Clarke KR, Harborne AR. Weighting species abundance estimates for marine
resource assessment. Aquat ConservMarine Freshw Ecosyst 1996;6:115–20.
Nalder IA, Wein RW. Spatial interpolation of climatic normals: test of a new method in
the Canadian boreal forest. Agr For Meteorol 1998;92:211–25.
Nasrollahzadeh HS, Bin Din Z, Foong SY. Trophic status of the Iranian Caspian Sea
based on water quality parameters and phytoplankton diversity. Cont Shelf Res
2008;28(9):1153–65.
National Academy of Sciences. Clean coastal waters: understanding and reducing the
effects of nutrient pollution. Washington: National Academy Press; 2003.
Naumann E. Nagra synpunkter angaende limnoplanktons okologi Med sarskild hansyn
till fytoplankton. Sv Bot Tidskr 1919;13:129–63.
Newton A, Icely JD, Falcao M, et al. Evaluation of eutrophication in the Ria Formosa
coastal lagoon, Portugal. Cont Shelf Res 2003;23:1945–61.
Nielsen SE, Bayne EM, Schieck J, Herbers J, Boutin S. A new method to estimate species
and biodiversity intactness using empirically derived reference conditions. Biol
Conserv 2007;137:403–14.
Nijboer RC, Verdonschot PFM. Variable selection for modelling effects of eutrophication
on stream and river ecosystems. Ecol Model 2004;177:17–39.
Nijkamp P, Voogd H. A survey of qualitative multiple criteria choice models. In: Nijkamp
P, Leitner H, Wringley N, editors. Measuring the unmeasurable. Dordrtecht: Kluwer
Nijhoff; 1986. p. 425–47.
Nikolaidis G, Patoucheas DP, Moschandreou K. Estimating breakpoints of chl-a in
relation with nutrients from Thermaikos Gulf (Greece) using piecewise linear
regression. Fresen Environ Bull 2006;15(9B):1189–92.
Nixon SW. Coastal marine eutrophication: a definition, social causes, and future
concerns. Ophelia 1995;41:199–219.
Nixon SW. Eutrophication and the macroscope. Hydrobiologia 2009;629:5-19.
Noakes D. Quantifying changes in British Columbia Dungeness crab (Cancer magister)
landings using intervention analysis. Can J Fish Aquat Sci 1986;43:634–9.
Nobre AM, Ferreira JG, Newton A, Simas T, Icely JD, Neves R. Management of coastal
eutrophication: integration of field data, ecosystem-scale simulations and
screening models. J Mar Syst 2005;56:375–90.
Nunneri C, Hofmann J. A participatory approach for Integrated River Basin Management
in the Elbe catchment. Estuar Coast Shelf S 2005;62:521–37.
OECD (Organization for Economic Cooperation and Development). Eutrophication of
waters, monitoring, assessment and control. Paris: OECD Publication; 1982.
Okolodkov YB, Dodge JD. Biodiversity and biogeography of planktonic dinoflagellates in
the Arctic Ocean. J Exp Mar Biol Ecol 1996;202:19–27.
Orfanidis S, Panayotidis P, Stamatis N. Ecological evaluation of transitional and coastal
waters: a marine benthic macrophytes-based model. Medit Mar Sci 2001;2(2):
45–65.
Orfanidis S, Panayotidis P, Stamatis N. An insight to the ecological evaluation index
(EEI). Ecol Indicat 2003;3(1):27–33.
OSPAR/ASMO.. Integrated assessments of inputs to the OSPAR Convention area 1990–
1996. Outcome of INPUT Special Assessment Workshop, The Hague. OSPAR
Commission Meeting Document ASMO 98/5/9; 1998.
O'Sullivan PE. Eutrophication. Int J Environ Stud 1995;47:173–93.
Paerl HW. Assessing and managing nutrient-enhanced eutrophication in estuarine and
coastal waters: interactive effects of human and climatic perturbations. Ecol Eng
2006;26:40–54.
Paerl HW, Valdes-Weaver LM, Joyner AR, Winkelmann V. Phytoplankton indicators of
ecological change in the eutrophying Pamlico Sound System, North Carolina. Ecol
Appl 2007;17:S88-S101.
Pagou K, Ignatiades L. Phytoplankton seasonality patterns in eutrophic marine coastal
waters. Biol Oceanogr 1988;5:229–41.
Painting S, Devlin M, Rogers S, Mills DK, Parker ER, Rees HL. Assessing the suitability of
OSPAR EcoQOs for eutrophication vs ICES criteria for England and Wales. Mar Pollut
Bull 2005;50:1569–84.
Parlamento Italiano. Decreto Legislativo 11 maggio 1999, n. 152, Allegato I.
Monitoraggio e Classificazione delle Acque in Funzione degli Obiettivi di Qualita
Ambientale. (www.parlamento.it); 1999.
Pearson TH, Rosenberg R. Macrobenthic succession in relation to organic enrichment
and pollution of the marine environment. Oceanogr Mar Biol Annu Rev 1978;16:
229–311.
Peters DPC, Bestelmeyer BT, Turner MG. Cross-scale interactions and changing pattern–
process relationships: consequences for system dynamics. Ecosystems 2007;10:
790–6.
Pettine M, Casentini B, Fazi S, Giovanardi F, Pagnotta R. A revisitation of TRIX for trophic
status assessment in the light of the European Water Framework Directive:
Application to Italian coastal waters. Mar Pollut Bull 2007;54(9):1413–26.
Pettit C, Pullar D. An integrated planning tool based upon multiple criteria evaluation of
spatial information. Comput Environ Urban Syst 1999;23:339–57.
Pielou EC. The interpretation of ecological data: a primer on classification and
ordination. New York: John Wiley & Sons; 1984.
Poole RW. An introduction to quantitative ecology. New York: McGraw-Hill; 1974.
Postma H. The cycle of nitrogen in the Wadden Sea and adjacent areas. Neth J Sea Res
1966;3(2):121–86.
Powell TM, Cloern JE, Huzzey LM. Spatial and temporal variability in South San
Francisco Bay (U.S.A.). I. Horizontal distributions of salinity, suspended sediments
and phytoplankton biomass and productivity. Estuar Coast Shelf S 1989;28:583–97.
Primpas I, Karydis M. Improving statistical distinctness in assessing trophic levels: the
development of simulated normal distributions. Environ Monit Assess 2010a, doi:
10.1007/s10661-009-1177-1.
Primpas I, Karydis M. Scaling the trophic index (TRIX) in oligotrophic marine
environments. Environ Monit Assess 2010b, doi:10.1007/s10661-010-1687-x.
Primpas I, Karydis M, Tsirtsis G. Assessment of clustering algorithms in discriminating
eutrophic levels in coastal waters. Glob Nest J 2008;10:359–65.
Primpas I, Tsirtsis G, Karydis M, Kokkoris GD. Principal component analysis:
development of a multivariate index for assessing eutrophication according to
the European water framework directive. Ecol Indicat 2010;10:178–83.
Raju KS, Duckstein L, Arondel C. Multicriterion analysis for sustainable water resources
planning: a case study in Spain. Water Resour Manage 2000;14:435–56.
Rast W, Jones RA, Lee GF. Predictive capability of U.S. OECD phosphorus loading–
eutrophication response models. J WPCF 1983;55((7):990-1003.
Reizopoulou S, Nikolaidou A. Benthic diversity of coastal brackish-water lagoons in
western Greece. Aquat ConservMarine Freshw Ecosyst 2004;14(S1):S93-S102.
Restrepo JD. Applicability of LOICZ catchment-coast continuum in a major Caribbean
basin: the Magdalena River, Colombia. Estuar Coast Shelf S 2008;77:214–29.
Revelante N, Gilmartin M. The relative increase of larger phytoplankton in a subsurface
chlorophyll maximum of the Northern Adriatic Sea. J Plankton Res 1995;17:1535–62.
Romesburg HC. Cluster analysis for researchers. North Carolina: Lulu Press; 2004.
Routledge RD. Diversity indices: which ones are admissible? J Theor Biol 1979;76:
503–15.
Salas F, Teixeira H, Marcos C, Marques JC, Pérez-Ruzafa A. Applicability of the trophic
index TRIX in two transitional ecosystems: the Mar Menor lagoon (Spain) and the
Mondego estuary (Portugal). J Mar Sci 2008;65(8):1442–8.
Scheffer M, Szabó S, Gragnani A, et al. Floating plant dominance as a stable state. Proc
Natl Acad Sci USA 2003;100(7):4040–5.
Schramm W. Factors influencing seaweed responses to eutrophication: some results
from EU-project EUMAC. J Appl Phycol 1999;11:69–78.
Shahrban M, Etemad-Shahidi A. Classification of the Caspian Sea coastal waters based
on trophic index and numerical analysis. Environ Monit Assess 2010;164:349–56.
Sharma S. Applied multivariate techniques. John Wiley & Sons, Inc; 1996.
Sheskin D. Handbook of parametric and nonparametric statistical procedures. Chapman
& Hall/CRC; 2004.
Shevyrnogov A, Vysotskaya G. Spatial distribution of chlorophyll concentration
seasonal dynamics types in the ocean based on the autocorrelation analysis of
SeaWiFS data. Adv Space Res 2006;38:2176–81.
Simboura N, Zenetos A. Benthic indicators to use in ecological quality classification of
Mediterranean soft bottom marine ecosystems, including a new biotic index. Medit
Mar Sci 2002;3/2:77-111.
Simpson EH. Measurement of diversity. Nature 1949;163:688.
Smith SV. Carbon–nitrogen–phosphorus fluxes in the coastal zone: the global approach.
IGBP Glob Change Newsl 2002;49:7-11.
Smith VH, Tilman GD, Nekkola JC. Eutrophication: impacts of excess nutrient inputs on
freshwater, marine and terrestrial ecosystems. Environ Poll 1999;100:179–96.
Soetaert K, Middelburg JJ. Modeling eutrophication and oligotrophication of shallow-
water marine systems: the importance of sediments under stratified and well-
mixed conditions. Hydrobiologia 2009;629:239–54.
 D. Kitsiou, M. Karydis / Environment International 37 (2011) 778–801
Sokal RR, Rohlf FJ. Biometry. New York: Freeman; 1981.
Spatharis S, Tsirtsis G. Ecological quality scales based on phytoplankton for the
implementation of Water Framework Directive in the Eastern Mediterranean. Ecol
Indicat 2010;10:840–7.
Steele JH. The structure of marine ecosystems. Cambridge: Harvard Univ. Press; 1974.
Stefanou P, Tsirtsis G, Karydis M. Nutrient scaling for assessing eutrophication: the
development of a simulated normal distribution. Ecol Appl 2000;10:303–9.
Stevens JP. Applied multivariate statistics for the social sciences. New Jersey: Lawrence
Erlbaum Associates, Inc., Publishers; 1996.
Stollenwerk N, Drepper FR, Siegel H. Testing nonlinear stochastic models on
phytoplankton biomass time series. Ecol Model 2001;144(2–3):261–77.
Stolte W, Graneli E. Threshold nutrient levels for harmful algal events in some European
coastal waters. THRESHOLDS: Thresholds of Environmental Sustainability, D3.1.2,
Sixth Framework Programme; 2006. http://www.thresholds-eu.org/.
Taebi S, Etemad-Shahidi A, Fardi GA. Examination of three eutrophication indices
to characterize water quality in the north east of Persian Gulf. J Coast Res 2005;42:
405–11.
Talaue-McManus L, Smith SV, Buddemeier RW. Biophysical and socio-economic
assessments of the coastal zone: the LOICZ approach. Ocean Coast Manage 2003;46:
323–33.
Tett P, Gilpin L, Svendsen H, et al. Eutrophication and some European waters of
restricted exchange. Cont Shelf Res 2003;23:1635–71.
Thingstad TF, Rassoulzadegan F. Nutrient limitations, microbial food webs, and ‘biological
C-pumps’: suggested interactions in a P-limited Mediterranean. Mar Ecol Prog Ser
1995;117:299–306.
Torbick N, Hu F, Zhang J, Qi J, Zhang H, Becker B. Mapping chlorophyll-a concentrations
in West Lake, China using Landsat 7 ETM+. J Great Lakes Res 2008;34(3):559–65.
Tsirtsis G, Karydis M. Evaluation of phytoplankton community indices for detecting
eutrophic trends in the marine environment. Environ Monit Assess 1998;50:255–69.
Tsirtsis G, Karydis M. Application of discriminant analysis for water quality assessment
in the Aegean. Samos, Greece: 6th Int Conf of Environmental Science and
Technology; 1999.
Tyson P, Steffen W, Mitra A, Fu C, Lebel L. The earth system: regional–global linkages.
Reg Environ Change 2001;2(3):128–40.
Underdal B, Skulberg OM, Dahl E, Aune T. Disastrous bloom of Chrysochromulina
polylepsis (Prymnesiophyceae) in Norwegian coastal waters 1988-mortality in
marine biota. Ambio 1989;18:265–70.
Underwood AJ. Techniques of analyses of variance in experimental marine biology and
ecology. Oceanogr Mar Biol Annu Rev 1981;19:513–605.
Underwood AJ. Experiments in ecology. Cambridge: Cambridge University Press; 2007.
UNEP. Assessment of the state of eutrophication in the Mediterranean Sea. Athens: MAP
technical reports series, no. 124; 1999.
UNEP. Eutrophication monitoring and strategy of MED POL. Athens: UNEP(DEC)/MED
WG.231/14; 2003.
UNEP. State of the Environment and Development in the Mediterranean Plan Bleu,
UNEP/MAP's Regional Agency Centre; 2009.
Vadrucci MR, Sabetta L, Fiocca A, et al. Statistical evaluation of differences in
phytoplankton richness and abundance as constrained by environmental drivers
in transitional waters of the Mediterranean basin. Aquat ConservMarine Freshw
Ecosyst 2008;18:S88-S104.
Valiela I. Marine ecological processes. New York: Springer-Verlag; 1995.
van Beusekom JEE. A historic perspective on Wadden Sea eutrophication. Helgol Mar
Res 2005;59(1):45–54.
Vascetta M, Kauppila P, Furman E. Aggregate indicators in coastal policy making:
potentials of the trophic index TRIX for sustainable considerations of eutrophica-
tion. Sust Dev 2008;16:282–9.
Vassiliou A, Ignatiades L, Karydis M. Clustering of transect phytoplankton collections
with a quick randomization algorithm. J Exp Mar Biol Ecol 1989;130:135–45.
Vázquez EV, Miranda JGV, Gonzalez AP. Characterizing anisotropy and heterogeneity of
soil surface microtopography using fractal models. Ecol Model 2005;182:337–53.
Vega M, Pardo R, Barrado E, Deban L. Assessment of seasonal and polluting effects
on the quality of river water by exploratory data analysis. Water Res 1998;32:
3581–92.
Verleyen E, Hodgson DA, Leavitt PR, Sabbe K, Vyverman W. Quantifying habitat-specific
diatom production: a critical assessment using morphological and biogeochemical
801
markers in Antarctic marine and lake sediments. Limnol Oceanogr 2004;49(5):
1528–39.
Vollenweider RA. Possibilities and limits of elementary models concerning the budgets
of substances in lakes. Arch Hydrolobiol 1969;66:1-36.
Vollenweider RA. Advances in defining critical loading levels for phosphorus in lake
eutrophication. Mem Ist Ital Idrobiol 1976;33:53–83.
Vollenweider RA. Eutrophication: a global problem. WHO Water Quality Bulletin, 6. ;
1981.
Vollenweider RA. Coastal marine eutrophication: principles and control. In: Vollenweider
RA, Marchetti R, Viviani R, editors. Marine coastal eutrophication. London: Elsevier;
1992. p. 1-20.
Vollenweider RA, Giovanardi F, Montanari G, Rinaldi A. Characterization of the trophic
conditions of marine coastal waters with special reference to the NW Adriatic Sea:
proposal for a trophic scale, turbidity and generalized water quality index.
Environmetrics 1998;9:329–57.
Voogd H. Multicriteria evaluation for urban and regional planning. London: Pion; 1983.
Vos RJ, Hakvoort JHM, Jordans RWJ, Ibelings BW. Multiplatform optical monitoring
of eutrophication in temporally and spatially variable lakes. Sci Total Environ
2003;312(1–3):221–43.
Vounatsou P, Karydis M. Environmental characteristics in oligotrophic waters — data
evaluation and statistical limitations in water-quality studies. Environ Monit Assess
1991;18:211–20.
Walz R. Development of environmental indicator systems: experiences from Germany.
Environ Manage 2000;25(6):613–23.
Wang JJ, Jing YY, Zhang CF, Zhao JH. Review on multi-criteria decision analysis aid in
sustainable energy decision-making. Renewable Sustainable Energy Rev 2009;13:
2263–78.
Warwick RM, Carr MR, Clarke KR, Gee JM, Green RH. A mesocosm experiment on the
effects of hydrocarbon and copper pollution on a sublittoral soft-sediment
meiobenthic community. Mar Ecol Prog Ser 1988;46:181–91.
Washington HG. Diversity biotic and similarity indices: a review with special relevance
to aquatic ecosystems. Water Res 1984;18:653–94.
Weber CA. Aufbau und Vegetation der Moore Norddeutschlands. Beiblatt Botanischen
Jahrbuchern 1907;90:19–34.
Weber D, Englund E. Evaluation and comparison of spatial interpolators. Math Geol
1992;24:381–91.
Weber DD, Englund EJ. Evaluation and comparison of spatial interpolators 2. Math Geol
1994;26:589–603.
Webster R, Oliver MA. Geostatistics for environmental scientists. Australia: John Wiley
and Sons; 2001.
Werdell PJ, Bailey SW, Franz BA, Harding Jr LW, Feldman GC, McClain CR. Regional and
seasonal variability of chlorophyll-a in Chesapeake Bay as observed by SeaWiFS and
MODIS-Aqua. Remote Sens Environ 2009;113(6):1319–30.
Wetzel RG. Limnology. Lake and river ecosystems. San Diego: Academic Press; 2001.
White DL, Porter DE, Lewitus AJ. Spatial and temporal analyses of water quality and
phytoplankton biomass in an urbanized versus a relatively pristine salt marsh
estuary. J Exp Mar Biol Ecol 2004;298:255–73.
Whittaker RH. Ordination of plant communities. London: W. Junk; 1982.
Xu FL, Tao S, Dawson RW, Li BG. A GIS-based method of lake eutrophication assessment.
Ecol Model 2001;144:231–44.
Zaldívar JM, Cardoso AC, Viaroli P, et al. Eutrophication in transitional waters: an
overview. Transit Waters Monogr 2008a;1:1-78.
Zaldívar JM, Strozzi F, Dueri S, Marinov D, Zbilut JP. Characterization of regime shifts in
environmental time series with recurrence quantification analysis. Ecol Model
2008b;210:58–70.
Zaldívar JM, Bacelar FS, Dueri S, Marinov D, Viaroli P, Hernández-García E. Modeling
approach to regime shifts of primary production in shallow coastal ecosystems.
Ecol Model 2009;220:3100–10.
Zhang H, Huang GH. Assessment of non-point source pollution using a spatial
multicriteria analysis approach. Ecol Model 2011;222:313–321.
Zitko V. Principal component analysis in the evaluation of environmental data. Mar
Pollut Bull 1994;28:718–22.
Zuur AF, Ieno EN, Smith GM. Analyzing ecological data. Springer; 2007.