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Fisheries Management and Ecology, 2007, 14, 381–392
Assessing the health of European rivers using
functional ecological guilds of fish communities:
standardising species classification and
approaches to metric selection
R. A. A. NOBLE & I. G. COWX
Hull International Fisheries Institute, University of Hull, Hull, UK
D. GOFFAUX & P. KESTEMONT
University of Namur, Namur, Belgium
Abstract The functional ecological guild approach is the cornerstone for the development of Indices of Biotic
Integrity and multi-metric indices to assess the ecological status of aquatic systems. These indices combine metrics
(unit-specific measures of a functional component of the fish community known to respond to degradation) into a
single measure of ecological assessment. The guild approach provides an operational unit linking individual
species characteristics with the community as a whole. Species are grouped into guilds based on some degree of
overlap in their ecological niches, regardless of taxonomic relationships. Despite European fish species having been
classified into ecological guilds, classification has not been standardised Europe-wide or within the context of
classifying species into guilds from which metrics can be developed for ecological assessment purposes. This paper
examines the approach used by the EU project FAME to classify European fish species into consistent ecological
guilds and to identify suitable metrics as basic tools for the development of a standardised ecological assessment
method for European rivers to meet the requirements of the Water Framework Directive.
KEYWORDS:
ecological guild, Europe, fish, Index of Biological Integrity, metrics, rivers.
Introduction
The Water Framework Directive as the basis for
harmonised ecological assessment methods
Implementation of the European Union Water Framework Directive (WFD) (EU 2000) as the standard
framework for water management within the European
Union requires harmonisation of ecological assessment
and the interpretation of the ecological status of water
bodies. Within the WFD, fish are one of the key quality
elements used to describe the ecological status of rivers.
Fish are good indicators of ecological status as they
occupy a wide range of ecological niches and operate
over a variety of spatial scales (Simon 1999). Consequently, fish have been used to develop community-
based indices that integrate a number of measures
(metrics) of functional community structure, linking
the ecological functions and requirements of different
species to the impacts of human pressures on the
structure and function of aquatic ecosystems (Simon
1999; Degerman, Beier, Breine, Melcher, Quataert,
Rogers, Roset & Simoens 2007). However, development of a standardised fish-based ecological assessment
method for European rivers will require harmonised
ecological classification and metric selection schemes as
basic tools. This paper describes the approach and
processes developed under the EU FAME project
(http://fame.boku.ac.at/) to classify European fish species into ecological guilds and to identify suitable
metrics as basic tools for the development of a new
standardised ecological assessment method.
Correspondence: Dr Richard Noble Hull International Fisheries Institute, University of Hull, Hull HU6 7RX, UK
(e-mail: [email protected])
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R. A. A. NOBLE ET AL.
The use of functional guilds in the assessment of
biotic integrity
Classification according to ecological and functional
guilds was developed to simplify community analysis
and assist in the prediction of community change
(Austen, Bayley & Menzel 1994). Root (1967) defined
guilds in the ecological sense as Ôa group of species that
exploit the same class of environmental resources in a
similar wayÕ. Evolution has determined that each fish
species has characteristic tolerances or preferences for
water quality, habitat and other environmental conditions. They have specific requirements for breeding,
feeding and growth. However, there is considerable
overlap in the requirements and traits of many species
that enables aggregation into larger functional units
with similar ecological characteristics. The use of
functional ecological guilds within the assessments of
ecological integrity is possible because of the relationships between fish community structure and the
functional complexity of riverine habitat (Goldstein
& Simon 1999; Welcomme, Winemiller & Cowx 2006).
The functional guild concept denotes that the fish
community structure is determined by the functional
diversity of the aquatic habitat, in terms of habitat
available and prevalent hydrological processes (similar
to river continuum concept, Vannote, Minshall, Cummins, Sedell & Cushing 1980). Within this, any changes
in, or disturbance to, the functionality and structure of
the riverine habitat will be reflected by responses in the
functional structure of the fish community.
Multi-metric indices comprise a number of metrics
measuring specific aspects from a range of guilds that are
known to respond in predictable ways to anthropogenic
disturbance to ecosystems. Therefore, guilds and metrics are inextricably linked, given that a metric is only a
unit-specific measure of a defined group of species within
a community. The discrimination of the dominant fish
species that characterise communities into an appropriate guild structure that yields robust metrics within an
index of biotic integrity (IBI) therefore requires good
levels of ecological understanding of species ecology and
behaviour. Additionally, the translation of guilds into
suitable metrics also requires an understanding of the
limitations of the method chosen to sample the fish
community, because these methods may be selective and
bias community structure and composition.
Selection and measurement of appropriate
ecological functions for an IBI
Since the first version of the IBI in North America by
Karr (1981), the IBI concept has been tested and/or
adapted for use throughout the world (for review, see
Miller, Leonard, Hughes, Karr, Moyle, Schrader,
Thompson, Daniels, Fausch, Fitzhugh, Gammon,
Halliwell, Angermeier & Orth 1988; Simon & Emery
1995; Hughes & Oberdorff 1999). The development of
IBIs has focussed on the combination of metrics
relating to the species composition, biological diversity, species abundance and condition (e.g. prevalence
of disease, hybrids and deformities) of fish communities. In most cases, the composition, diversity and
abundance measures assess the functional diversity of
the community. As such, metrics relating to habitat
guilds, trophic guilds and reproductive guilds have
been widely used. Whilst habitat, feeding and reproductive classifications have formed the key elements of
functional assessments, a number of other criteria have
been included. Classifications relating to the native
status of species, their life-history characteristics (longevity and migration) and tolerance to stresses of
various forms (e.g. pollution) have also been used in
IBIs. In this context, metrics can change with the
purpose of the index. If, for example, changes due to
pollution are to be detected, one would use metrics
sensitive to contaminants. In each new version, the list
of metrics changes more or less with the target region,
country or river type. Few of these metrics were used in
all versions (number of species, proportion of omnivores, presence of damages and diseases), but most
were specifically adapted to the features of ichthyofauna in the different countries, regions or river types.
The selection of metrics was based on different criteria,
such as biological importance (primary describers of
the ichthyofauna status), statistical importance
(selected according to their respective loading in
multivariate analyses), literature references (selected
by other authors), expert judgement (describing some
regional disturbances of rivers or features of specific
ichthyofauna) or specific applications (sensitive to
specific anthropogenic degradations). However, as yet
there has been no consistent approach to metric
selection for development or modification of IBIs.
Classification of ecological guilds and metrics
Given that classification and understanding of the
ecological functioning of a target fish community is a
prerequisite for the development of any IBI, the
development of a standardised ecological assessment
tool to aid the implementation of the WFD requires
that European fish species be classified in a harmonised
way. Therefore, for each of the six main ecological
functions identified in previous IBIs (trophic, reproduction, habitat, migration, longevity and tolerance),
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FUNCTIONAL ECOLOGICAL GUILDS OF FISH COMMUNITIES
this paper reviews the existing classifications for the
associated ecological guilds, identifies the relevant
ecological hypotheses for their inclusion within an
IBI and discusses the limitations that exist for each
group of guilds. In addition, the applications of metrics
pertaining to individual (sentinel) species that may
exhibit responses to degradation, and could be useful
within an ecological assessment, are discussed. Finally,
given the extent of species introductions and translocations across Europe, the potential differences
between alien and native species within metrics are
considered.
Ecological classification and metric selection
Trophic guilds
Fish display a wide range of feeding habits and occupy
many trophic roles from detritivores to secondary
carnivores. However, it is rare for fish to specialise in
one particular food category throughout their entire
life cycle. Furthermore, many species show ontogenetic
shifts in dietary preferences and plasticity in their
feeding behaviour depending upon ambient conditions. Although this variability and plasticity could
severely limit the powers of IBIs, trophic guilds have
been consistently used in the development of IBIs.
Theoretically, any changes that affect the structure and
availability of food resources and/or feeding habitats
alter the trophic guild structure of a fish community. In
general, perturbation to the aquatic environment will
tend to impact negatively on species with specialist
feeding requirements (e.g. insectivores and piscivores),
but favour those with flexible or diverse feeding
behaviour (e.g. omnivore).
Feeding classifications have developed through a
variety of approaches, including combinations of
dietary constituents, modes of feeding and feeding
habitat. Goldstein & Simon (1999) proposed a feeding
classification for North American freshwater fishes
comprising five main feeding guilds and 26 modes of
feeding. This classification was too complex for European fish fauna and the ecological information available. Furthermore, within the European context, few
fish species have specialist feeding habitats, and these
are mainly piscivores in the sub-adult and adult life
stages. This represents a potential limitation to the use
of feeding guilds. Consequently, a simplification was
required, in which trophic guilds were defined using
dominance of food items in the diet as the assessment
criterion (Table 1).
Classification systems that comprise elements of
dietary preference together with complementary feeding information, such as mode or habitat, have the
potential to overlap with other guild classifications,
especially that of habitat. The definition of benthivore
is a good example, as this is not a true characterisation
of diet and overlaps with the habitat guild. The
definition in Table 1 categorises benthivore as Ôconsisting of a high proportionÕ of benthic organisms. As
such, it uses both a habitat-related definition, but also
to some extent a food type definition. It is recognised
that some benthivores may also, technically, be placed
into one of the other categories, e.g. omnivore, if only
food type is used in the definition. Consequently, the
benthivore category also covers by the guild describing
habitat preference. Further confusion arises between
true benthivore habits and detrital feeding habits.
Benthivore should be limited to molluscs and macroinvertebrates. Detrital feeders often include a range of
smaller organisms in their diet. Ideally, in a classification based on the composition of the diet, when
identifying species with narrow trophic niches from
generalist species with wide niches, the benthivore
Table 1. Proposed trophic guild classification for European fishes
Guild
Planktivores
Herbivores
Detritivores
Omnivores
Insectivores/
invertivores
Benthivores
Piscivores
Parasite
Adult diet
Physiology/comment
High proportion of zooplankton and/or
phytoplankton
High proportion of plant material
High proportion of detritus
Diet ÔgeneralistÕ, including a wide range
of flora and fauna
High proportion of invertebrates/insects
Fine gill-rakers, elongated pharyngeal teeth, no stomach, and elongated
undifferentiated intestine
Terminal/sub-terminal mouth, bony slashing jaw, long digestive tract
Digestive tract simple/unspecialised
High proportion of benthic organisms
Ventro-terminal, often highly protractile mouth. File-like teeth to comb
and sort small organisms
Restricted to obligate piscivores
Consists of >75% fish
Parasitic feeding mode
Terminal/supra-terminal mouth, feed in the whole of the water column
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category would be omitted. However, given the limited
trophic data for some species, the benthivore category
is often retained in classification schemes. The same
problems hold true for other categories.
Difficulties in classification also arise with fish
species that change their trophic status over the course
of their lives, which link to ontogenetic niche shifts,
change in habitat preference/occupancy and changes in
diet based on availability and food partitioning. Data
regarding ontogenetic shifts in diet are too variable
and uncertain to be meaningful for inclusion in a
standardised system for broad-scale IBI development.
Consequently, classification must be limited to the
trophic guild of adults, the life stage for which most
data are available. Although this is a limitation, it
remains the best option until better definitions of
trophic guilds of each life-history stage are available.
Finally, once provisionally classified, many European freshwater fish species do not fall into discrete
categories, but also are not true omnivores. This is
most prevalent for species that exhibit distinct trophic
shifts or ranges of potential trophic status. In these
circumstances, the species can be classified into joint
groups, e.g. insectivore/piscivore. Such joint classifications are necessary to separate the ÔobligateÕ piscivores
(e.g. Esox lucius L.) from species whose diet may
include a high proportion of fish but do not solely rely
on a piscivorous diet [e.g. salmonids, Anguilla anguilla
(L.), Perca fluviatilis L.]. This is necessary because IBIs
often use omnivore and piscivore metrics. Furthermore, species such as eel and trout switch between
insectivorous and piscivorous diets under certain
conditions and this may mask the response of metrics
to degradation. Within an IBI, the species classification
should not change under different ecological conditions (either natural or due to perturbation). Again,
this type of classification is required to separate the
species within specific feeding guilds from those that
have wide dietary ranges.
Reproductive guilds
Fish exhibit diverse forms of reproduction, with
species showing different spawning behaviour and
using diverse spawning habitats. Consequently, reproductive guild classifications have been used within fishbased IBIs to assess changes in the structure of
communities, linked to changes in the availability of
different types of habitat. In many assessment methods, the lithophilic guild (gravel-spawners) and phytophilic guild (vegetation spawners) are used as
measures of the reproductive structure of fish communities. The theory behind using these guilds is that as
levels of degradation increase the availability and
suitability of specific niches or spawning substrata are
reduced, having a knock-on effect on the reproduction
of species with specific spawning requirements, e.g. the
loss or compaction of gravels results in a reduction in
the contribution of lithophils to the community.
Balon (1975) classified fish into 33 reproductive
groups based on ontogeny, spawning behaviour and
place of egg deposition. This classification scheme was
considered inappropriate for the development of guilds
for ecological assessment because many of the categories are for marine or tropical species. Also, Simon
(1999) considered that assigning species to the correct
reproductive guild is problematic because of paucity of
behavioural and early ontogenetic data, although this
is not necessarily true for European fishes, the reproductive ecologies of which are generally well known.
For the purposes of developing a typology for European riverine fishes, a simplified system of reproductive
guilds was developed (Table 2), based on the classification proposed by Balon (1975) and modified by
Table 2. Proposed system of classification of reproductive guilds
Guild
Spawning habitat
Lithophils
Phytophils
Phytolithophils
Psammophils
Ostracophils
Pelagophils
Lithopelagophils
Clean gravel, rocks, stones, rubble or pebbles
Plants, leaf and roots of live or dead vegetation
Submerged plants, if available, or on other submerged items
Roots or grass above a sandy bottom or on the sand itself
Shells of bivalve molluscs
Pelagic zone
Rocks and gravels
Ariadnophlis
Speleophils
Viviparous
Polyphils
Specialised nest building species
Interstitial spaces and crevices
NA
Non-specialised spawners no preferred habitat
Comment
Includes redd cutters
Pelagic embryos/larvae. Eggs initially
adhesive but soon become buoyant
May include some level of parental care
Live bearers
No specialised behaviour
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FUNCTIONAL ECOLOGICAL GUILDS OF FISH COMMUNITIES
Chadwick (1976), Mahon (1984), Bruton & Merron
(1990), Oberdorff & Hughes (1992), Boet, Chessel,
Hugueny, Oberdorff, Pont & Porcher (1999) and Cowx
(2001). The classification was primarily based on
preferred spawning habitat as this fits well with the
requirements and structure of IBIs.
A range of assessment metrics (Table 2) were
identified that relate to reproductive guilds, including
both reproductive habitat and specialised behaviour.
Ariadnophilic, speleophilic, viviporous and polyphilic
were included to the basic Ôreproductive habitatÕ guild
classification to account for the slightly more specialised (or non-specialised in the case of polyphils)
behaviour of certain European species (Table 2).
Habitat guilds
Each fish species has optimal habitat requirements,
which result in changes in community structure along
the upstream–downstream gradient of a river. These
habitat requirements have long been recognised and
used to classify different zones in a river (Huet 1959;
Hawkes 1975) inhabited by different fish species with
similar habitat preferences. It is widely acknowledged
that the size, vitality and spatial distribution of species
are dependent on the quantity and quality of their
habitat (Karr 1991). Fish have been classified according to habitat use by numerous authors (e.g. Schlosser
1982; Leonard & Orth 1986; Bain, Finn & Booke 1988;
Lobb & Orth 1991). However, many assessments of
habitat preference are limited to the regions in which
they were developed and are too specific for general
use within an IBI.
The habitat assessment within an IBI is generally
designed to assess the morphological condition and
hydrological functioning of the river. As such, classification schemes for habitat preference generally consider flow preferences (e.g. Schiemer & Waidbacher
1992; Aarts & Nienhuis 2003). The classifications
developed include assessment of the rheophilic, eurytopic or limnophilic preferences, together with subgroups based on migration and spawning and juvenile
habitat (in terms of backwaters) requirements. Aarts &
Nienhuis (2003) discriminated six categories based on
these two elements, therefore doubling up with other
classification criteria, such as reproductive and migration guilds. Ideally, a guild system used within an IBI
would not have guilds described by different ecological
functions. Therefore, the habitat guild structure proposed uses only three groups: rheophilic (all freshwater
life stages confined to lotic waters) eurytopic (all life
stages can occur in both lentic and lotic waters) and
limnophilic (all life stages confined to lentic waters).
Further combinations of guilds within IBIs can be
achieved by computing metrics from a combination of
guilds.
In most IBIs, metrics relating to the abundance or
diversity of limnophilic and rheophilic species are used
as a measure of the effects of impoundment and
channelisation of rivers, which alter both the magnitude and variability of flow. Channelised and
impounded rivers usually result in reductions in water
velocity, which favours limnophilic/eurytopic species
over those with rheophilic preferences. Alternatively,
where a lowland river channel has been channelised
and/or isolated from its floodplain by flood defence
works, the abundance and number of limnophilic/
eurytopic species will be reduced. This is especially
important for the eurytopic species that rely on
secondary channels and floodplain water bodies for
reproduction.
An additional two-group classification based on
feeding habitat, either water column (prefer to live and
feed in the water column, usually do not go to the
bottom to search for food) or benthic (prefer to live on
or near the bottom, from where they take food, and
usually do not go to the surface for feeding purpose),
was suggested by Karr (1981). He used darter species
to represent those sensitive to degradation of benthic
habitats, and sunfish as those sensitive to changes in
water column habitats. However, this guild may
prove redundant because of the complimentary nature
of the classification (i.e. a species can only be one or
the other), the overlaps with trophic guilds and the
problem of vertical scale dependent upon river zone.
The vertical scale in shallow upland rivers is much less
than that of deeper, lowland rivers, and, consequently,
true benthic or water column species may only occur in
the deeper lowland sections where the vertical spatial
scale allows differentiation.
Life-history strategies: migration guilds
Ecological guilds for residency/migratory life histories
are important because absence of migratory species,
where they once existed, suggests a bottleneck at one
or all stages of the life cycle, possibly caused by
environmental perturbation or obstruction to movement. Migratory species, therefore, give potential for
an assessment of the condition of a river system in
terms of connectivity (Schmutz & Jungwirth 1999).
However, despite the importance of connectivity (both
longitudinal and lateral) to the functioning of fish
communities, few IBIs have attempted to integrate
metrics based on the assessment of migration guilds.
Migratory behaviour of fish in rivers can be divided
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into two major types: potadromy and diadromy, the
former referring to that occurring entirely within the
inland waters of a river system (Northcote 1999), and
the latter to that taking place across a transition zone
between fresh and marine waters (McDowall 1997).
Diadromy can be further divided into three subcategories:
Anadromy (running up rivers) refers to fishes that
live as older juveniles and sub-adults in the sea but at
maturity migrate up rivers to spawn, e.g. Atlantic
salmon, Salmo salar L.
Catadromy (running down rivers) refers to fishes
that live all their early life in fresh water – feeding and
growing – but at maturity migrate downstream to
spawn in the sea, e.g. anguillid eels.
Amphidromy (running between rivers and the ocean)
refers to fishes that spend appreciable parts of their life
in both fresh and sea waters, feeding and growing in
both, and whose migrations seem to have no direct
relationship to reproduction (McDowall 1997).
Assessment of the species that exhibit these different
migration strategies can give valuable information to
assessments of the ecological condition of rivers.
However, categorisation of migration guilds is not as
distinct as it first appears, and some species, e.g. Salmo
trutta L., exhibit a range of migratory traits having
both iteroparous and semelparous life histories. These
complexities in migratory behaviour give rise to
problems in standardised classification schemes as a
species may exhibit different migratory behaviours in
different river types.
Four main classes are proposed based on migration
strategy and scale; short, intermediate, long-anadromous and long-catadromous. Short and intermediate
migration classes cover potadromy over different
spatial scales, whilst long migration categories cover
all anadromous and catadromous migration. Short
migrations cover species that only moved within a
particular river zone, whereas intermediate migration
covers species with potadromous migrations between
river zones (i.e. within river migration on a larger
spatial scale, e.g. barbel, Barbus barbus (L.), and
bream, Abramis brama (L.). However, for some
euryhaline species [such as shads, Alosa alosa (L.)
and Alosa fallax (Lacepède)] the migrations are only
over an intermediate spatial scale, but are anadromous. Therefore, a fifth class, intermediate anadromous, was designated for these species.
The scheme above relates to longitudinal migration. However, many species exhibit lateral migration
behaviour between main river channels, side channels
and floodplain waters, especially in lowland rivers
(Aarts & Nienhuis 2003). The status of these species
gives an indication of the morphological condition of
the river channel and its connectivity with the active
floodplain (Welcomme 1979; Grift, Buijse, Breteler,
Van Densen, Machiels & Backx 2001; Aarts, Van
Den Brink & Nienhuis 2004). Therefore, any scheme
to classify migration should reflect the overall
connectivity of a river system and include scope
for classification of lateral migration requirements of
floodplain species. Lateral migration requirements
are, however, difficult to assess for many species,
given a lack of understanding and the impacted
nature of many European floodplains. For the
purposes of an IBI approach, the use of metrics
concerning the status of limnophilic and eurytopic
species in river systems, species requiring lotic
floodplain waters for some or all of their life cycle,
is considered adequate for assessing lateral connectivity.
Life history: longevity and maturation guilds
Many IBIs have used classifications relating to longlived species to assess the ecological status of fish
communities. These measures are designed to give
some assessment of different life-history strategies (e.g.
K and r strategies, Pianka 1970). Karr (1981) proposed
that the status of long-lived species could integrate
disturbances to the aquatic environment over multiple
years. Additionally, the absence or low abundance of
species with different life-history patterns may indicate
different types of disturbance, or provide evidence of
either acute or chronic environmental disturbance.
However, classification of longevity, as a coarse
measure of life history, is variable across Europe,
and needs harmonisation. A longevity scheme comprising short-lived (typically < 5 yr), intermediate (5–
15 yr) and long-lived species (>15 yr) gives scope for
the development of metrics for ecological assessment.
In addition, within this scheme the early/late maturation of long-lived species can be formalised as 625%
of the life span, giving some measure of life-history
strategy. However, the longevity and age at maturation
of each species can also be a reflection of the
geographical location of the population within its
natural range, the stability of the habitat and the
optimal/sub-optimal nature of the habitat. Some
species have great plasticity and can adapt their life
histories to survive under different conditions (e.g.
Cowx 1990). Furthermore, longevity is highly correlated with maximum size reached (Pauly 1980).
Therefore, ultimately the applicability of these types
of classifications to ecological assessments may be
limited.
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FUNCTIONAL ECOLOGICAL GUILDS OF FISH COMMUNITIES
Tolerance capacity guilds
Assessment of the tolerance of species to anthropogenic pressures has commonly been used in ecological
assessment. The theory behind the use of tolerance
guilds is intolerant species will be present/thrive in
good conditions but absent under disturbed conditions, where tolerant species will dominate/thrive.
Classifications based on the tolerance or intolerance
of species to perturbations in water quality (eutrophication and/or acidification) (e.g. Alabaster & Lloyd
1982) and habitat have been used in previous IBIs
developed for Europe. Breine, Simoens, Goethals,
Quataert, Ercken, Van Liefferinghe & Belpaire (2004)
presented a scheme for water bodies in Flanders
scoring tolerance to water quality and habitat degradation on a five-point scale, with 1 being the most
tolerant and 5 the most intolerant. They then calculated an overall tolerance score for each species as an
average of the values assigned for tolerance to
individual pressures. Oberdorff, Pont, Hugueny &
Porcher (2002) empirically defined tolerant species
for an IBI for French rivers using indices of water
quality and habitat flexibility, as defined by Verneaux
(1981) and Grandmottet (1983) respectively. Despite
both schemes presenting individual scores for the
species flexibility, Oberdorff et al. (2002) and Aarts &
Nienhuis (2003) concluded that ultimately classification was restricted to three groups; tolerant, intermediate and intolerant. It is probable that, despite
published schemes and recent research, lack of understanding of ÔtoleranceÕ, especially that of Ôoverall
toleranceÕ, restricts classification to only coarse interpretations of tolerant, intolerant and intermediate.
Despite the apparent logic for assessing tolerance,
the value and validity of the use of tolerance guilds has
not been evaluated. This is especially true where
tolerance is classified based on apparent flexibility in
ecological requirements. Where ÔtoleranceÕ is based on
ecological flexibility, suitable habitat and trophic guild
classifications could make ÔtoleranceÕ guilds redundant.
Furthermore, the apparent tolerance of a certain
species to a particular variable will depend upon the
location of the species within its geographical range: a
species in sub-optimal conditions on the edge of its
range is likely to be more sensitive to an additional
stressor than it would be under optimal conditions. In
addition, the use of Ôoverall toleranceÕ, a simple
combination of tolerances to specific pressures, may
be an invalid classification given that the mechanisms
of response of different species to different pressures
will be variable. Furthermore, the sensitivity of species
to specific pressures is complex under natural condi-
tions, given that in many cases both habitat and water
quality degradation are concurrent. Despite these
problems with tolerance classification, an overall
tolerance guild was included, based on classifications
of tolerance to eutrophication, acidification and habitat degradation.
Type-specific sensitive species: Ôsentinel Õ species
The classification of high, good and moderate ecological status, as prescribed in the text of the WFD, takes
into account the presence, abundance and population
structure of Ôtype-specific sensitive speciesÕ. As such,
any method developed to assess ecological status for
the WFD should consider the population structure of
type-specific sensitive species. This would require
definition of Ôtype-specificÕ and ÔsensitiveÕ. As a simpler
alternative, a number of species can be identified as
ÔsentinelÕ species, i.e. those species that are deemed to
be indicative of a particular river zone, but also those
that will provide information on ecological status.
Consequently, the sentinel species were defined as
those that are relatively common within the specific
river type and for which electric fishing is not size
selective. In Western Europe, the key species are
generally dominant and associated species for river
reaches according to the Huet zonation scheme (Huet
1959). For these key species, information regarding
recruitment and population structure should be
assessed. As such, a range of metrics variants could
be defined and tested for a number of life stages or age
classes of these sentinel species. With detailed ecological knowledge, these life stages could then be classified
into different ecological guilds. However, ecological
information pertaining to ontogenetic shifts in ecology
is often limited. Therefore, for sentinel species the
easiest approach was to develop metrics for youngof-the year individuals that would provide an indication of the levels of recruitment within the population.
Fish species distribution, residency and historical
status of fish species
Some IBIs have used metrics relating to the historical
status of fish species to derive fish community typologies and define reference conditions for ÔpristineÕ
ecological status (Schmutz, Kaufmann, Vogel, Jungwirth & Muhar 2000). In these cases, it has been
argued that the development of an IBI requires clear
definition of fish species that actually reflect ambient
environmental conditions based on natural residency.
This classification is important because species have
now been widely introduced (e.g. rainbow trout),
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translocated or have become extinct in many regions
(e.g. burbot, Lota lota (L)) in the UK; Welcomme
1992; Cowx 1997). Introductions and extinctions of
species reflect major changes to community compositions and pose significant problems for rehabilitation.
This is especially true where species introductions can
have serious implications for the resident fish community. In such cases, introductions and stocking can
alter the structure of the community, away from a
reference condition that does not include the alien
species, to a state that is not easy to rectify. However,
the impacts of species introductions on the ecological
status of rivers are not dealt with explicitly by the
WFD. Consequently, due accord needs to be given to
the residency status of species and the role they take in
establishing reference conditions and assessing status.
Given that alien species also have characteristic ecological traits and are subject to the same environmental
pressures, they may respond to degradation in the
same way as the native community. However, many
introduced species are generally tolerant, which may
limit their response to degradation pressures. Moreover, introduced species often persist at low densities
until the environment changes, after which they can
replace more specialised native species and become a
pest. Therefore, the development of new methods
should test metrics for both native and alien species. In
this case, each metric, defined for each ecological guild,
has further variants relating to whether all species or
only native species are considered within each guild.
The residency status of each fish species in each
European drainage basin was compiled. Species were
classified as native, introduced (translocated from
within Europe), introduced to Europe, or endemic [to
country, specific eco-region (as defined by Illies 1978)
or river basin]. Where known, the date of any
introduction was recorded. Any significant translocations of species between water bodies within each
country were also recorded. It should be noted that in
some regions, despite knowing a species was alien, the
period that had elapsed since the introduction (many
hundreds of years in some cases) meant that some alien
species were deemed to be naturalised on a national
level (e.g. common carp, Cyprinus carpio L., in
Western Europe). As such, many ÔalienÕ species that
have become naturalised over a long period of time are
regarded as ÔnativeÕ and managed accordingly. However, to allow the metrics relating to alien and native
species to be tested, if a species was not historically
present in the river basin concerned it was considered
an alien. This classification was expanded into a river
basin/river region-specific scheme to allow the development of ichthyo-graphical regions within Europe
(Reyjol, Hugueny, Pont, Bianco, Beier, Caiola, Casals,
Cowx, Economou, Ferreira, Haidvogl, Noble, De
Sostoa, Vigneron & Virbickas 2007) for use in the
development of standardised assessment methods
(Pont, Hugueny & Rogers 2007).
Conclusions
Ecological guilds
Even with a simplified ecological classification scheme,
lack of understanding of the ecological functions and
requirements of species limits their accurate classification into guilds. This lack of ecological knowledge
results in a high proportion of European freshwater
fish species being unclassified (Table 3). Overall, only
123 of the 236 species recorded in the countries covered
by the FAME project could be classified in all of the
ecological functions; trophic, reproductive, habitat,
migration, tolerance and longevity. Furthermore,
when considering the key ecological functions of
trophic, habitat and reproductive traits only 155 of
the 236 species could be classified. Twenty-nine species
had no ecological trait information. The functions with
the lowest rate of classification were tolerance and
migration. This probably highlights a lack of understanding of potadromous migration behaviour and
limited understanding of the tolerance of species to
perturbation.
Gaps in ecological information and classification
potentially pose serious problems to ecological assessments, especially if a marked proportion of a community is excluded from the assessment because they are
not classified into guilds. These gaps in knowledge
need to be addressed to strengthen the basic foundations of guild-based ecological assessment methods.
Furthermore, gaps in knowledge for key ecological
functions need to be addressed. Classification of
migration behaviours can form the basis of assessments of ecological connectivity within river systems.
However, it is apparent that the migration patterns
and requirements of many potamodromous species are
not well understood. This is probably due to the
widespread impoundment of European rivers, which
has occurred for many centuries. The lack of natural,
un-degraded systems with free migratory access, limits
interpretation of natural migration patterns.
The lack of knowledge is especially true for species
assemblages in the relatively unexplored river basins of
Europe, e.g. The Balkans and Aegean peninsular.
Furthermore, many of these river systems exhibit very
different hydrological processes, e.g. intermittent flow
regimes, compared with rivers of Northern Europe.
2007 The Authors. Journal compilation 2007 Blackwell Publishing Ltd
FUNCTIONAL ECOLOGICAL GUILDS OF FISH COMMUNITIES
Table 3. Summary of the numbers of European freshwater fish
species classified into the main guilds of each ecological function and
the number of species that remain unclassified
Ecological
function
Trophic
Reproductive
Habitat
Feeding
Migration
Tolerance
Longevity
Overall
Main guilds
Insectivore/Invertivore
Benthivore
Omnivore
Unclassified
Lithophils
Phytophils
Phytolithophils
Unclassified
Rheophilic
Eurytopic
Limnophilic
Unclassified
Benthic
Water column
Unclassified
Long Migratory Anadromous
Long Migratory Catadromous
Intermediate distance migrations
(Potadromy)
Unclassified
Tolerant
Intolerant
Intermediate tolerance
Unclassified
Long-lived
Intermediate life span
Short-lived
Unclassified
Total number of species
Classified all functions
Classified key functions
(trophic, habitat, reproduction)
No ecological data
Number of
species/taxa
31
36
52
59
75
36
19
59
69
35
79
53
97
73
65
16
2
39
70
34
33
89
80
58
61
57
60
236
123
155
29
Classification based on expert panel assessment of published and
grey literature.
There is potential for these different hydrological
regimes to translate into distinct functional ecologies
and life histories for the endemic fauna of Southern
Europe (see Magalhães, Beja, Canas & CollaresPereira 2002). As such, a simplified guild structure
developed primarily for Northern Europe may not be
suitable for southern species assemblages. However,
for many of these endemic species and species assemblages, a lack of ecological data limits an assessment of
the suitability of this simple guild structure. Furthermore, in many cases the taxonomic classification of
these species assemblages is still debatable.
Assessment of some ecological functions highlighted
great plasticity within populations and between populations across their range. This is especially true with
feeding guilds. Ideally, feeding guilds should be omitted from ecological assessments in their current format
(Welcomme et al. 2006). Any development of feeding
guilds needs to assess the plasticity in dietary habits of
the species rather than purely the predominant food
type. Furthermore, assessments of tolerance, particularly Ôglobal toleranceÕ, are vague and should be
replaced by more suitable assessments of their plasticity in ecological functions. However, until additional
ecological knowledge is available, the designation of
tolerant and intolerant species will provide reasonable
classification of species with known reaction to human
pressure, but for which the mechanisms of reaction are
not fully understood.
Metric selection
Review of the metrics previously used in North
America and Europe suggest they assess the same
aspect of a functional community, but measure them in
different ways. Consequently, three criteria must be
used during the selection process: ecological suitability,
statistical robustness and methodological criteria. For
example, the metric Ôbenthic speciesÕ can be used to
assess one functional aspect of the community and its
changing status with degradation, but there are many
ways of measuring it: number of benthic species
present, proportion of benthic species present, number
of individuals, proportion of individuals, biomass or
proportion of biomass of benthic species. The analytical technique used to measure the metric must be
suitable to the requirements of the fish-based index, the
structure of the community being studied, the ability to
define a reference condition and the ease of classification and scoring of the metric within the observed
range of values. This is a matter of ecological and
statistical sensitivity of the metric chosen. The measure
used must be sensitive enough to detect changes in the
feature or function of the community being assessed.
Overlaid on these criteria are criteria developed from
an understanding of sampling and data limitations.
Selection of metrics must therefore be justified at three
levels and satisfy a range of criteria at each level. Any
metric chosen must ultimately be backed up by:
• ecological reasons for choosing the metric, a hypothesis for the reaction of the metric to degradation;
• statistical reason for the measurement used (ability
to categorise and score the range of values observed
against a valid reference condition);
• understanding of the limitations of the sampling
procedure used to assess the metric.
In conclusion, the main criterion for selecting the
most relevant metrics is that a candidate metric (in
2007 The Authors. Journal compilation 2007 Blackwell Publishing Ltd
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R. A. A. NOBLE ET AL.
Figure 1. Schematic of potential metrics belonging to the species composition category that should be tested in the development of an index of biotic
integrity. For each guild all potential metrics variants are indicated. * indicates that Ôspecialised speciesÕ excludes lithophilic and phytophilic species.
terms of a guild or ecological function) should be
proposed in relation to the expected variation with
degradation. Once this list of candidate metrics is
identified, all potential variants of the metrics should
be tested rather than merely choosing one or a couple
of options. An example of the matrix of potential
metrics relating to species composition is presented in
Figure 1. In the matrix, the guilds identified are those
selected from a hypothesis for their response to
degradation and the multitude of unit measurements
are all variants that should be tested statistically.
Acknowledgements
Many thanks are due to all the members of the FAME
consortium who contributed to the harmonised classification, particularly N. Roset, J. de Leuw, E. Winter,
R. Haberbosch, J. Breine, E. Degerman J. Oliveira,
M. Lapinska, T. Virbickis, A. Melcher, N. Caiola and
R. Barbieri. We would like to thank the European
Commission for funding the FAME project (EVK1CT-2001-00094).
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