Hydrobiologia (2017) 787:27–44

DOI 10.1007/s10750-016-2974-5

REVIEW PAPER

Functional diversity: a review of methodology and current

knowledge in freshwater macroinvertebrate research
Dénes Schmera . Jani Heino . János Podani . Tibor Er}os . Sylvain Dolédec

Received: 16 June 2016 / Revised: 25 August 2016 / Accepted: 27 August 2016 / Published online: 7 September 2016
Ó The Author(s) 2016. This article is published with open access at Springerlink.com

Abstract Although several studies have examined diversity measures have been applied for quantifying
the functional diversity of freshwater macroinverte- functional diversity of freshwater macroinvertebrate
brates, the variety of methodologies combined with assemblages, among which Rao’s quadratic entropy
the absence of a synthetic review make our under- looks like the most frequent. In most papers, func-
standing of this field incomplete. Therefore, we tional diversity was positively related to taxon rich-
reviewed the current methodology for assessing ness, and functional redundancy was a key concept in
functional diversity in freshwater macroinvertebrate explaining this correlation. Most studies detected
research. Our review showed that most papers quan- strong influence of the environmental factors as well
tified functional diversity using biological traits, as human impact on functional diversity. Finally, our
among which feeding habits were the most common review revealed that functional diversity research is
traits probably due to the assumed links between biased towards European running waters and is
feeding and ecosystem functions. A large number of hindered by yet insufficient information on the aute-
cology of macroinvertebrates.

Keywords Environmental variables
Functional

Electronic supplementary material The online version of redundancy
Human impact
Taxonomic resolution

this article (doi:10.1007/s10750-016-2974-5) contains supple- Traits
mentary material, which is available to authorized users.

Handling editor: Judit Padisák

J. Podani
D. Schmera (&)
T. Er}os Department of Plant Systematics, Ecology and
MTA Centre for Ecological Research, Balaton Theoretical Biology, Institute of Biology, L. Eötvös
Limnological Institute, Klebelsberg K. 3, Tihany 8237, University, Budapest, Hungary
Hungary
e-mail: [email protected] J. Podani
MTA-ELTE-MTM Ecology Research Group of the
D. Schmera Hungarian Academy of Sciences, Eötvös University,
Section of Conservation Biology, University of Basel, Budapest, Hungary
Basel, Switzerland
S. Dolédec
J. Heino CNRS, UMR 5023 - LEHNA, Biodiversité et Plasticité
Natural Environment Centre, Finnish Environment dans les Hydrosystèmes, Université Lyon 1,
Institute, Oulu, Finland 69622 Villeurbanne, France

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28 Hydrobiologia (2017) 787:27–44

Introduction (Violle et al., 2007), or specific mouthpart characters

of aquatic insects might predict feeding specific food
In response to the growing threat of biodiversity loss in items (Cummins, 1974). Thanks to the terminological
virtually all ecosystems, much effort has been devoted clarification made by plant ecologists, traits reflecting
to exploring and predicting the consequences of the effects of organisms on ecosystem functions are
anthropogenic disturbance in ecological communities. collectively called as ‘effect traits’ (Violle et al., 2007)
In spite of the increasing number of studies, it is still and functional diversity should quantify the variability
unclear how biological diversity and ecosystem func- or diversity of these effect traits (Fig. 1).
tioning are governed under natural conditions and how Plant ecologists also suggested that the perfor-
they are impacted by human activity (Reiss et al., mance and the existence of species in a given
2009). Increasing number of experiments have shown environment depend on ‘response traits’ (Violle
that biodiversity enhances, rather than simply et al., 2007). Linking this idea to the habitat templet
responds to ecosystem functions (Balvanera et al., theory of Southwood (1977) suggests that environ-
2006; Cardinale et al., 2009). mental variables can be considered as filters, which
Community ecologists and conservation biologists constrain organisms. As a result, the response traits are
have quantified several facets of diversity simultane- properties of organisms, which allow them coping
ously within species assemblages (Devictor et al., with different environmental conditions (see e.g. Poff,
2010). Of these, taxonomic diversity is the most 1997). Within this theoretical framework, the response
commonly considered, but it does not fully represent of functional diversity to environmental variables and
phylogenetic and functional differences among spe- to human impact is an indirect and rather complex
cies. Phylogenetic diversity incorporates differences mechanism (Fig. 1).
in the evolutionary history of species. Finally, func- Macroinvertebrates (i.e. invertebrate animals [
tional diversity relies on those components of biodi- 0.25 mm in length, Rosenberg & Resh, 1993) play
versity that influence how an ecosystem operates or an important role in freshwater ecosystems by feeding
functions (Tilman et al., 1997). Consequently, it is the on algae, coarse detritus or fine particulate organic
facet of diversity that provides the link between matter (i.e. contributing to carbon and nitrogen
ecosystem functioning and biodiversity (Petchey & cycles), by engineering (Mermillod-Blondin, 2011;
Gaston, 2006). As such, Cadotte et al. (2011) and Statzner, 2012) and by providing food for higher
Gagic et al. (2015) reviewed functional diversity trophic levels, such as fish (Covich et al., 1999).
measures to bring to the fore emerging ecological However, our knowledge on the way functional
patterns and provide clues about ecosystems manage- diversity of macroinvertebrate assemblages influences
ment and decision-making. Their literature reviews patterns and processes in freshwater ecosystems needs
indicate that functional diversity is one of the best to be broadened. Small-scale experimental studies
predictors of ecosystem function. have suggested that the species richness of
According to our current understanding, the effect
of biodiversity on ecosystem functioning is manifested
through traits, where a trait is ‘‘a well-defined, ENVIRONMENT ORGANISMS FUNCTIONS
measurable property of organisms, usually measured Environmental Response Effect
at individual level and used comparatively across variables traits traits
Ecosystem funcon 1
species’’ (McGill et al., 2006). More generally, a set of
traits determines where a species can live (see Lavorel
Ecosystem funcon 2
et al., 1997). Ideally, these properties would include
process rates (i.e. resource consumption rates), or
should reflect specific abilities of organisms (e.g. the ? Funconal
Habitat templet diversity
existence of specific digestive enzymes). In most
cases, however, such information is not available and Human impact ?
only surrogates of species functions are applied. For Fig. 1 Schematic representation of the relationships between
instance, specific leaf area (the ratio of leaf area to leaf functional diversity, response and effect traits and related terms
mass) is a good surrogate of net photosynthetic rate (see text for further explanation)

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Hydrobiologia (2017) 787:27–44 29

macroinvertebrates drives ecosystem functioning Literature survey

(Cardinale et al., 2002; Frainer et al., 2014), whereas
recent reviews have drawn a more complex picture On 28th April 2015, we performed a literature search
based on field studies (Lecerf & Richardson, 2010; in ISI Science Citation Index Expanded database from
Vaughn, 2010; Dolédec & Bonada, 2013). In partic- 1900 to 2014 with the following combination of
ular, the link between ecosystem functioning and relevant keywords: (‘‘functional diversity’’ OR ‘‘func-
biodiversity depends on a cascade effect among tional richness’’ OR ‘‘functional evenness’’ OR ‘‘func-
species’ dominance and identity, the existence of tional divergence’’ or ‘‘functional regularity’’ OR
positive interactions among species, sequence of ‘‘functional complementarity’’ OR ‘‘functional spe-
species loss, species traits and the environmental cialization’’ OR ‘‘functional dispersion’’ OR ‘‘func-
context (e.g. Vaughn, 2010). Vaughn (2010) also tional redundancy’’) AND (‘‘invertebrat*’’ OR
argued that successful prediction of linkages between ‘‘macroinvertebrat*’’). This search resulted in 297
biodiversity and ecosystem functioning requires a records. Then, after examining the abstracts, only
multitude of empirical approaches. Finally, studies papers related to freshwater assemblages and ecosys-
looking at the biodiversity ecosystem-functioning (B- tems were retained (i.e. studies dealing with marine,
EF) relationship have usually been assessed at the lagoon or estuary ecosystems and the functional
local scale, and therefore the results do not apply diversity of enzymes were disregarded), which
directly at a regional scale (Dolédec & Bonada, 2013). reduced the number of papers to 90. Finally, each
Our review focuses on macroinvertebrate assem- paper was read carefully to check its relevance to
blages of freshwater habitats, while those of marine macroinvertebrate biodiversity and community ecol-
ecosystems or brackish waters are beyond our scope. ogy in freshwater realms. Twelve papers were irrel-
Although studies regarding these realms overlap to evant. Thus, we ended up with 78 relevant papers of
some extent, freshwater and marine sciences have which 6 were reviews (all of these papers are cited in
developed more or less independently. Note that we the reference list). The earliest of the 78 papers was
have only considered entire assemblages and their published in 2000.
biodiversity, rather than individual or infra-individual
levels of organization (see Literature survey).
Although ‘‘functional diversity’’ and related terms How functional diversity is conceptualized
are frequently used in studies of freshwater macroin- and measured?
vertebrate assemblages, the terminology used and the
concept itself may lack consistency and mathematical Recent reviews clearly show that functional diversity
clarity, which can cause confusions (see Schmera has been given a wide variety of conceptual and
et al., 2014, 2015). In addition, our present knowledge methodological definitions (Petchey et al., 2004;
is based on separate case studies appearing as inde- Botta-Dukát, 2005; Mason et al., 2005; Mouillot
pendent snapshots. However, disentangling how func- et al., 2005; Ricotta, 2005; Petchey & Gaston, 2006;
tional diversity of freshwater macroinvertebrate Ricotta & Moretti, 2008; Villéger et al., 2008; Poos
assemblages is governed under natural conditions, et al., 2009; Laliberté & Legendre, 2010; Mouchet
while potentially also influenced by human stressors, et al., 2010; Schleuter et al., 2010). Here, our aim is not
remains challenging (Fig. 1, see also Dolédec & to compile yet another overview on the strong and
Statzner, 2010). As former reviews in freshwater weak points of the different concepts and measures—
ecology have mostly dealt with trait–environment it has been made by the authors cited above. Instead,
relationships (Bonada et al., 2006; Heino et al., 2013), we attempt to explain the complex nature of the
the present paper focuses on (i) how functional various terms, which have appeared in association
diversity is conceptualized and quantified, (ii) to what with studies on functional diversity of freshwater
extent taxonomic and functional diversity are corre- macroinvertebrate assemblages. In doing this, we treat
lated, (iii) how functional diversity responds to the terms concept and measure separately. The term
environmental variables and human impact and finally concept will be used in a broad sense referring to
(iv) whether functional diversity drives ecosystem general ideas and the term measure as a mathematical
functions and, if so, which ones. expression for quantifying a biological property (for

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example, conceptualized as functional diversity). In communities. Hence, functional redundancy has

this section, we detail key concepts having primary strong implication in biological conservation because
importance in functional diversity research, namely it may compensate for losses of ecosystem functioning
functional diversity, functional richness, functional after a decline in species richness. Nevertheless,
evenness, functional divergence, functional redun- functional redundancy also has some limitations. By
dancy, functional complementarity and functional examining fish faunas of tropical reefs, Mouillot et al.
contribution (Table 1), while measures will be dis- (2014) observed high functional redundancy com-
cussed later. bined with high functional vulnerability: some unique
combinations of functional traits were represented by
Concepts used in macroinvertebrate studies a single species. If two species have different roles,
then these species complement each other and the
Mason et al. (2005) suggested that functional diversity concept describing their functional difference is
comprises three primary components: functional rich- known as functional complementarity (Petchey,
ness, functional evenness and functional divergence. 2003). Finally, functional contribution is the func-
Although the recent literature uses these terms both as tional value (or contribution) of species to the
concepts (i.e. different conceptual aspects of func- functional diversity of communities (Schmera et al.,
tional diversity) as well as measures (when the 2009b).
mathematical expression provided by the developers From our literature survey, functional diversity was
are followed), in this section we adhere to the former the most frequently used term (59 hits out of 78
meaning. Functional richness is defined as the amount records) followed by functional redundancy (17),
of trait space occupied by the species, functional functional richness (11) and functional divergence
evenness relates to the distribution of abundances in (5). Rarely occurring concepts were functional even-
the trait space, whereas functional divergence ness (3), functional complementarity (3) and func-
expresses how the abundance distribution maximizes tional contribution (1). That is, freshwater ecologists
difference in the trait space (Mason et al., 2005; have considered several concepts of functional diver-
Mouillot et al., 2005). sity in a rather unbalanced manner. The high fre-
The concept of functional redundancy is based on quency of the terms like functional redundancy and
observations that some species perform similar roles richness suggests that freshwater macroinvertebrate
in communities and ecosystems, and may therefore be research is focused on how species can replace each
substituted with no or very little impact on ecosystem other regarding ecosystem functions (functional
processes (Rosenfeld, 2002; Dolédec & Bonada, redundancy) and on the proportion of the unique
2013). For example, Bêche & Statzner (2009) and functions (functional richness). This is an obvious
Statzner et al. (2004) demonstrated that strong habitat indication that functional diversity research is usually
filters prevailing in streams of the USA and Europe oriented towards applied ecology and conservation
promoted functional redundancy in invertebrate biology.

Table 1 Main concepts of functional diversity research and their short definition
Concept Definition

Functional diversity Components of biodiversity that influence how an ecosystem operates (Tilman et al., 1997)
Functional richness Amount of functional trait space occupied by the species (Mason et al., 2005)
Functional evenness Distribution of abundance among functional characters (Mason et al., 2005)
Functional redundancy Situation when two or more species have the same function in the community (Rosenfeld, 2002)
Functional divergence Degree to which the abundance distribution maximizes differences in functional characters within
the community (Mason et al., 2005)
Functional complementarity Functional difference of two or more taxa (Petchey, 2003)
Functional contribution Individual value of species to the functional diversity of the community (Schmera et al., 2009b)

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Do we use mathematically defined terms? variable that is characterized by one element of a set of
distinguishable states (Schmera et al., 2015). Gather-
The 78 papers were read carefully to check whether ing information on the functional roles of freshwater
functional diversity or related terms have received macroinvertebrates is a challenging task, and apart
mathematical definitions. More than half of the papers from the availability of information, there is no
(40) used mathematical definitions, whereas a high consensus on which traits (or features) of macroin-
proportion of the papers (38) did not (e.g. Charvet vertebrate taxa should be used to calculate functional
et al., 2000; Statzner et al., 2005; Dolédec & Statzner, diversity. In this section, we first review the most
2008; Brouard et al., 2012). Papers without mathe- frequently used groups of traits and, second, we
matical definitions include reviews, because reviews overview the development of functional diversity
generally focused on new findings rather than method- research in the last 15 years.
ology (e.g. Heino et al., 2013). In other papers without The first conceptual model on the functional role of
mathematical definitions, functional diversity was freshwater macroinvertebrates is attributable to Cum-
interpreted as functional differences among taxa mins (1974). He studied streams from a functional
without precise mathematical definition (e.g. Mermil- perspective and described the processing of particulate
lod-Blondin et al., 2002), or functional diversity was and dissolved organic matter. Macroinvertebrates
used only as a keyword (e.g. Mermillod-Blondin et al., were central to his model, which distinguished
2004). Noticeably, the number of papers studying between species feeding on coarse or fine particulate
functional diversity, as well as that of papers using organic matter, grazing on periphyton and capturing
mathematical terms has increased since 2000 (Fig. 2). live prey. From a theoretical point of view, this model
In our view, this is a clear indication that functional provided the basis for subsequent and successful river
diversity is treated in our field both as a concept and a ecosystem concepts (e.g. Vannote et al., 1980).
measure. We do not have any objection against this, Twenty years later after the original proposal by
but researchers should keep in mind the dual meaning, Cummins (1974), the research team studying the
and clearly separate concept from measure and recall Upper Rhône River (hereafter referred to as the
that some measures have been shown to perform better ‘‘Rhône group’’; see Chevenet et al. 1994; Dolédec
than others in terms of biodiversity–ecosystem func- & Statzner, 1994; Statzner et al., 1994; Usseglio-
tion relationship (Flynn et al., 2011). Polatera, 1994) pioneered the use of species traits to
characterize entire floodplain communities and to
Which traits should be used to characterize examine trait–environmental variability relationships.
functional diversity? The team’s major objective was to use long-term
research made on the Upper Rhône for testing the
Traits in freshwater macroinvertebrate research habitat templet concept of Southwood (1977). This
include a wide variety of features, where trait is a concept, adapted to river systems by Townsend &
Hildew (1994), suggests that the temporal disturbance
and spatial heterogeneity of the river habitats provide
the frame for characteristic species traits to evolve.
Within their framework, biological traits included
maximal body size, potential number of descendants
per reproductive cycle, potential number of reproduc-
tive cycles per individual, reproductive technique,
parental care, distance travelled with or against the
current, attachment to soil or substrate, body form and
flexibility, resistant life stages, potential for regener-
ation, food types, feeding habits and respiration. On
Fig. 2 Changes in the number of papers published from the the other hand, habitat requirements described repro-
examination of the functional diversity of freshwater macroin-
ductive period, tolerance to variation in humidity and
vertebrates from 2000 to 2014. Full dots show the total number
of papers while empty dots show the number of papers using variability in habitat use. In parallel to this work,
mathematically defined terms Usseglio-Polatera et al. (2000) and Tachet et al. (2010)

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developed a trait database for European invertebrate should not be used for assessing functional diversity
genera including ‘‘biological traits’’ such as maximum because ecological traits should be regarded as
body size, life span, number of reproduction cycles per response traits (Violle et al., 2007), and response
year, types of aquatic stages, reproduction technique, traits are not directly linked to ecosystem functions
dispersal, resistance forms, respiration mode, loco- (Fig. 1, but see indirect effects in Frainer et al., 2014).
motion and substrate relation (hereafter referred to We should note, however, that the idea of effect and
locomotion), food types and feeding habits. They also response traits was developed in the context of plant
provided ‘‘ecological traits’’ or habitat requirements ecology, and the categorization of traits strongly
including lateral and longitudinal distribution, altitu- depends on the actual situation. In the case of
dinal and substrate preferences, current velocity, freshwater invertebrates, the clear separation of
trophic status, salinity and temperature preferences, response and effect traits is rather challenging in
saprobic values and tolerance to low pH. We should practice. Authors studying the functional diversity of
emphasize, however, that these traits were suggested freshwater macroinvertebrate assemblages used all
for improving the mechanistic understanding of biological traits (Bady et al., 2005; Peru & Dolédec,
species–environment relationships and not for quan- 2010), but mostly traits related to feeding habits
tifying functional diversity per se. In addition, the (Nhiwatiwa et al., 2009; Schmera et al., 2009a, b;
assignment whether a trait is biological or ecological Kadoya et al., 2011; Podani et al., 2013), size and
largely depends on the authors. For example, Mondy feeding habits (Pavoine & Dolédec, 2005) and feeding
& Usseglio-Polatera (2014) recently considered bio- habits, locomotion and substrate relation (Heino,
logical traits such as maximal body size, life span, 2005, 2008; Heino et al., 2008). The frequent occur-
number of reproductive cycles per year, types of rence of macroinvertebrate feeding habits is not
aquatic stages, reproduction technique, dispersal, surprising since they are, as already indicated, directly
resistance forms, respiration mode, locomotion and related to important ecosystem functions in freshwater
substrate relation (hereafter referred to locomotion), ecosystems. Regarding the other side of the coin and
food types and feeding habits as Eltonian traits, without questioning the importance of feeding habits
whereas ecological traits such as lateral and longitu- in quantifying functional diversity, we should also
dinal distribution, altitudinal and substrate prefer- emphasize that other biological traits may provide
ences, current velocity, trophic status, salinity and useful information on ecosystem functioning (e.g.
temperature preferences and saprobic values and body size predicts a very large proportion of variabil-
tolerance to low pH were termed Grinnellian traits. ity of any process rate; see e.g. Lecerf & Richardson,
Here, we follow Usseglio-Polatera et al. (2000) 2011; or several traits are involved in export of prey
terminology and use these terms as biological and animals to terrestrial environments through insect
ecological traits. emergence). Therefore, we argue that macroinverte-
In quantifying functional diversity, we found that brate researchers should not restrict themselves to
most papers (28) used only biological traits (including studying only feeding habits-related resource con-
only a subset of biological traits), whereas a small sumption, but recommend the examination of other
proportion of the papers (8) used both biological and functions provided by macroinvertebrates in freshwa-
ecological traits. Ecological traits included the above ter and terrestrial ecosystems. We also suggest that (1)
set of Grinnellian traits (Usseglio-Polatera et al., 2000; further autecological studies are needed for quantify-
Colas et al., 2013); rheophily and thermal preference ing additional and more expressive effect traits of
(Poff et al., 2006; Milner et al., 2011; Brown & Milner, macroinvertebrates, and (2) functional and trait diver-
2012); rheophily alone (Colzani et al., 2013); temper- sity should clearly be separated: the first is an
ature, pH, trophic status, longitudinal distribution, ecosystem function-related term using only effect
microhabitat and current velocity preferences (Marti- traits, while the second has no such restrictions.
nez et al., 2013) and substrate preferences (Vaz et al.,
2014). Although we do not state that the conclusions Measuring functional diversity
drawn from these studies are incorrect, we argue
following Verberk et al. (2013) that ecological traits The various ways for measuring functional diversity in
describing habitat preferences of macroinvertebrates the papers selected from our literature survey include

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14 measures, mainly delivered from terrestrial ecol- Paillex et al., 2013; Reynaga & Dos Santos, 2013). In
ogy. Here, we present the chronological appearance of 2014, almost all reviewed papers used Rao’s quadratic
these measures in order to demonstrate the develop- entropy for measuring functional diversity of fresh-
ment of this field. water macroinvertebrates (e.g. Boersma et al., 2014;
Feld et al., 2014; Kovalenko et al., 2014; Lange et al.,
Shannon diversity, richness and evenness 2014; Vaz et al., 2014).

Usseglio-Polatera et al. (2000) applied the Shannon Number of unique combinations of trait states
diversity index commonly used to quantify taxonomic
diversity (Magurran, 2004), to macroinvertebrate Functional diversity measures discussed until now
groups defined from the traits of taxa (mostly genera). consider traits as independent variables. However,
Several forthcoming papers used the Shannon formula Poff et al. (2006) argued that individual traits of
for quantifying functional diversity of freshwater freshwater macroinvertebrate taxa are inter-dependent
macroinvertebrates (Haybach et al., 2004; Devin due to phylogenetic (evolutionary) constraints. To
et al., 2005; Heino, 2005; Bazzanti et al., 2009). In handle this inter-dependency of traits, they measured
addition to Shannon diversity, Heino (2008) and functional diversity as the number of unique combi-
Göthe et al. (2014) considered functional richness nations of trait states (Poff et al., 2006). This measure
and functional evenness. counts the entities (individuals or taxa) differing in
(the combination of) trait states. Consequently, the
Rao’s quadratic entropy unit of this diversity measure is the pattern (combi-
nation) of trait states. This concept was used under the
Following Champely & Chessel (2002), Pavoine & name ‘‘unique trait combinations’’ in Schmera et al.
Dolédec (2005) used Rao’s quadratic entropy (Rao, (2012) and Schmera et al. (2013). In agreement with
1982) for measuring functional diversity of freshwater the original proposal (Poff et al., 2006) and following
macroinvertebrate assemblages. Bady et al. (2005) the recommendation of Schmera et al. (2015), this
demonstrated that functional diversity accumulation measure should be called ‘‘number of unique combi-
curves saturated faster than species richness accumu- nations of trait states’’.
lation curves, a first illustration of the potential
functional redundancy within freshwater invertebrate Number of trait states
assemblages (see also Bêche & Statzner, 2009). Rao’s
quadratic entropy incorporates the pairwise distances Bêche & Resh (2007) and Bêche & Statzner (2009)
of taxa weighted by their relative abundances and proposed to count the number of trait categories as a
appears to be a weighted version of Simpson diversity measure of functional diversity. This measure was also
index. Consequently, the measure is the expected used as ‘‘number of traits present’’ (see Milner et al.,
distance between two randomly selected individuals 2011) or should be called as ‘‘number of trait states’’
(Ricotta, 2005). According to Mason et al. (2005), following the terminology of Schmera et al. (2015).
Rao’s quadratic entropy quantifies the divergence This measure disregards evolutionary constraints but
aspect of functional diversity (see also Brown & focuses on traits assumed to be subject to selection.
Milner, 2012). Pavoine & Dolédec (2005) argued that The same concept was used when trait states were
Rao’s quadratic entropy has an obvious advantage represented by functional group identities (Gallardo
over usual diversity indices because, in addition to et al., 2009, 2014; Nhiwatiwa et al., 2009). In this
incorporating differences in traits, it takes into account respect, functional feeding group identities, and in fact
the abundance differences between species. There is the functional feeding groups, are integral parts of the
no doubt that Rao’s quadratic entropy has become the trait-based analyses.
most frequently used measure of functional diversity
by occurring in 19 of 40 papers that defined functional Simpson diversity
diversity mathematically (e.g. Peru & Dolédec, 2010;
Vandewalle et al., 2010; Colas et al., 2011; Gallardo Bêche & Resh (2007) applied the Simpson diversity
et al., 2011; Buendia et al., 2013; Graeber et al., 2013; function (Magurran, 2004) to the frequency-

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distribution of abundance-weighted categories for Kadoya et al., 2011; Patrick & Swan, 2011; Brown &
each trait, and the average measure was termed as Milner, 2012; Colzani et al., 2013; Martinez et al.,
trait diversity, whereas Gallardo et al. (2009) calcu- 2013). According to Mason et al. (2005), dendrograms
lated the same index for abundance-weighted func- quantify the functional richness aspect of functional
tional groups of macroinvertebrates. If applied to diversity.
functional diversity, it is less sensitive to rare
functional groups than Shannon diversity (Ricotta & Functional divergence and dispersion
Szeidl, 2006).
Quantifying the functional diversity of aquatic insects
Average pairwise distance and MFAD in the Atlantic Forest (Brazil) with dendrograms,
Colzani et al. (2013) considered functional divergence
Bêche & Resh (2007) also used the average pairwise and functional dispersion. The authors defined func-
trait-distance between taxa after Heemsbergen et al. tional divergence as an aspect of functional diversity
(2004), who used this measure for the first time. It is that enumerates the degree to which an abundance
easy to see that this measure is insensitive to the distribution maximizes divergence (or differences) in
abundance of the taxa. functional characters within the community (Mason
There are other measures disregarding abundance. et al., 2005; Mouillot et al., 2005). They further
For instance, studying functional attribute diversity defined functional dispersion as the spread of species
(FAD) measured through the sum of pairwise dissim- within the functional space (see Laliberté & Legendre,
ilarities of traits among taxa (Walker et al., 1999), 2010). Both measures have rarely been used in
Schmera et al. (2009a) recognized that the measure quantifying the functional diversity of freshwater
was extremely sensitive to the number of species and macroinvertebrate assemblages (e.g. Frainer et al.,
increased upon addition of a new species if it was 2014).
functionally identical to another one already present in
the community. As a remedy, Schmera et al. (2009a) Combinatorial functional diversity
developed a new measure termed as ‘‘modified FAD’’
(or MFAD). According to Colas et al. (2013), MFAD Recently, Podani et al. (2013) argued that not only
quantifies functional divergence. Until now, MFAD unique trait states could quantify functional diversity
has been used only in a few papers examining (see also Poff et al., 2006), but functional diversity can
freshwater macroinvertebrate communities (Schmera also rely upon the frequency distribution of trait
et al., 2009b; Colas et al., 2013). combinations. The methodological framework pro-
posed by the authors is based on information theory
Dendrogram-based measure and includes several terms like combinatorial func-
tional diversity, combinatorial functional evenness,
Petchey & Gaston (2002) derived the measurement of combinatorial functional richness, functional associa-
functional diversity using dendrograms from phylo- tum as well as functional heterogeneity (Podani et al.,
genetic diversity research. The dendrogram-based 2013). Other authors in freshwater science, probably
measure includes the following three steps: (1) due to a relative new publication and methodology,
calculating the functional trait dissimilarity matrix of have not yet used this combinatorial functional
taxa, (2) obtaining the dendrogram from this dissim- diversity framework.
ilarity matrix by cluster analysis, and (3) quantifying
functional diversity of the community as the total Convex hull
branch length of the dendrogram. Although the
original idea provoked intensive debate on how Boersma et al. (2014) recently examined invertebrate
dendrograms should be used for quantifying func- assemblages of pools in arid-land streams and quanti-
tional diversity (Podani & Schmera, 2006, 2007; fied functional richness by the volume of a convex hull
Petchey & Gaston, 2007, 2009), several papers have (i.e. the smallest polyhedron that encloses the points
used them for quantifying functional diversity of representing species in the functional trait space). This
freshwater assemblages (Vidakovic & Palijan, 2010; measure was proposed by Villéger et al. (2008) and

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criticized by Podani (2009) because zero or near zero independently from taxonomic diversity (Reynaga &
convex hull volumes might be obtained independently Dos Santos, 2013). This trend follows Cadotte et al.
on how wide the individual trait ranges are. (2011) who showed that the positive relationship
Our review shows that of the 14 measures, Rao’s between species richness and functional diversity is
quadratic entropy is the most frequently used measure not supported in every case. They argued that func-
for quantifying functional diversity of freshwater tional redundancy, type of traits used for quantifying
macroinvertebrates (Fig. 3). This suggests that, in functional diversity, type of functional diversity
most cases, functional diversity is interpreted as the measures and the strength of environmental filters
expected distance between two randomly selected can all influence the relationship between taxon
individuals. In addition to this clear interpretation, the diversity and functional diversity.
success of this measure could be explained by the facts Functional redundancy is a key factor in explaining
that this measure was the first to incorporate traits of the taxon richness–functional diversity relationship. A
freshwater macroinvertebrates into the direct mea- high number of functionally unique species leads to a
surement of functional diversity (Shannon diversity is linear relationship between taxonomic and functional
based on groups of taxa where traits are used indirectly diversity, whereas a high number of redundant species
for producing groups) and that this measure was causes a saturating relationship. Poff et al. (2006)
frequently used by members of the ‘‘Rhône group’’, recognized that only a limited number of unique trait
who have attained a leading role in trait-based states are represented in stream macroinvertebrate
research. Further frequently used measures are the assemblages having high functional redundancy
Shannon diversity, dendrogram-based measures and (Bêche & Resh, 2007; Bêche & Statzner, 2009; Brown
the number of trait states (Fig. 3). & Milner, 2012). In agreement with this finding,
Boersma et al. (2014) demonstrated experimentally
that due to high functional redundancy, drying did not
How functional diversity is related to taxonomic affect functional richness or functional diversity of
diversity? stream macroinvertebrates. Mueller et al. (2013) also
argued that functional diversity measured through trait
Most of the surveyed studies showed positive rela- (state-) richness shows limited variability.
tionship between taxon diversity and functional Three independent studies using different measures
diversity (Haybach et al., 2004; Bêche & Resh, proved that the functional diversity of freshwater
2007; Heino, 2008; Bazzanti et al. 2009; Bêche & macroinvertebrates presents relatively high stability
Statzner, 2009; Vandewalle et al., 2010; Gallardo and converges to the maximum faster than species
et al., 2011; Feld et al., 2014), while others revealed a richness in the function of sampling effort (Bady et al.,
positive and saturating relationship (Bady et al., 2005; 2005; Schmera et al., 2009a; Peru & Dolédec, 2010).
Bêche & Statzner, 2009). Finally, a single paper These findings can be explained by the functional
stated that functional diversity fluctuates fairly redundancy within the community.

Fig. 3 Frequency
distribution of the measures
used for quantifying
functional diversity of
freshwater
macroinvertebrates

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36 Hydrobiologia (2017) 787:27–44

Heino et al. (2008) and Gallardo et al. (2011) biological traits in the assemblages (Dolédec et al.,
examined the relationship among different diversity 2000; Gayraud et al., 2003; but see Waringer et al.,
measures (including functional ones) for freshwater 2013). Thus, genus level seems to be a good
macroinvertebrate assemblages. They found that compromise between sufficient taxonomic resolution
even if functional diversity correlated with some, and available biological trait information. However,
but not all, biodiversity measures, correlations were studies are still silent on how taxonomical resolution
not high enough to guarantee that any biodiversity influences functional diversity measures. We hence
measure could replace functional diversity. They suggest that the effects of taxonomic resolution on
concluded that each index quantifies a unique aspect variation in different functional diversity measures
of biodiversity, and the use of multiple measures will be examined in future studies.
might describe the multi-faceted aspect of biodiver- Most studies examining the functional diversity of
sity more appropriately, a feature in accordance with freshwater macroinvertebrates are based on identifi-
findings in terrestrial ecosystems (see e.g. Mouchet cation over the species level. A recent study by
et al., 2010). Waringer et al. (2013) showed that contrasting
characters of species are disregarded when species
are aggregated to genera or families (see also Tachet
On the role of taxonomic resolution et al., 2010), and thus handling genera and especially
and autecological knowledge in shaping functional families as homogeneous units may prevent from the
diversity research real functional diversity value of communities. Using
this example, we by no means state that identifica-
Our literature survey revealed that only three papers tion at higher ranks is useless or the findings based
used species-level identification to assess functional on these data are misleading, but emphasize that
diversity, focusing on one (Schmera et al., 2009a, b) more detailed autecological knowledge at the species
or two insect orders (Pavoine & Dolédec, 2005), level would strengthen our understanding on func-
while the majority of the papers applied mixed tional diversity of freshwater macroinvertebrate
taxonomic resolutions, with most individuals being assemblages. Most importantly, the biological trait
identified at genus or family levels. The appropriate information is biased towards the most abundant
taxonomic resolution to be used in macroinvertebrate species, which are easy to collect and study, whereas
studies, a broad zoological group, has been the knowledge is often lacking for rare species (Dolédec
subject of many papers (see e.g. Lenat & Resh, & Statzner, 2010).
2001). One explanation is that, in most taxonomic Our literature survey on the functional diversity of
groups, species are rather difficult to identify at early freshwater macroinvertebrates is biased towards
life stages. In addition, larvae of less known groups Europe and North America, while South America,
of freshwater macroinvertebrates are also difficult to Africa, Asia, Australia and Oceania are underrepre-
identify at the species level (e.g. Chironomidae). sented (Fig. 4). This global unevenness should
There are considerable advances in autecological
information on macroinvertebrates identified in
Europe at species level (Schmedtje & Colling,
Europe
1996; Moog, 2002; Hering et al., 2004; Furse
North America
et al., 2006; Schmidt-Koiber & Hering, 2015).
However, autecological information is often lacking South America
for many species due, for example, to their small Africa
abundance and thus being less studied (see Supple- Asia
mentary Table 1 for some trait databases). As Australia and Oceania
autecological information is measurable at individual
level, we do not see any theoretical objection against 0 5 10 15 20 25 30
Frequency
the use of taxonomical resolution higher than species
level. In a few studies, macroinvertebrates identified Fig. 4 Frequency distribution of the paper origins in the
at genus level accurately described the variation of different continents

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Hydrobiologia (2017) 787:27–44 37

encourage research in the latter continents. Regarding How functional diversity responds
habitat types, research is also biased, because streams to environmental variables and to human impacts?
(including rivers) are overrepresented (36 of 40
papers), while ponds (2) and lakes (2) are exemplified Most, but not all, studies suggest that functional
by much fewer papers. All of these suggest that most diversity of macroinvertebrate assemblages responds
of our knowledge is originated from the study of to different environmental factors (Table 2). The most
European and North American streams, and this bias likely explanation for this dependence is that individ-
might influence our synthesis. ual species are sensitive to environmental filtering

Table 2 Case studies explaining the response of functional diversity to environmental variables
Habitat Predictor variable Response variable Effect Reference

Headwater stream pH, mosses, nitrogen, colour, Shannon richness Significant Heino (2005)
substratum
Headwater stream pH, canopy Shannon diversity Significant Heino (2005)
Headwater stream Canopy, colour Shannon evenness Significant Heino (2005)
Lake littoral Macrophytes, lake surface area, Shannon richness Significant Heino (2008)
substratum characteristics
Lake littoral Macrophytes, lake surface area, Shannon diversity Significant Heino (2008)
hardness, total phosphorus
Lake littoral Hardness, colour, macrophytes, Shannon evenness Significant Heino (2008)
total phosphorus
Pond Mesohabitat Shannon diversity Significant Bazzanti et al. (2009)
River floodplain Hydrological connectivity among Number of trait states Significant Gallardo et al. (2009)
river channels
River floodplain Hydrological connectivity among Simpson diversity Significant Gallardo et al. (2009)
river channels
Stream % fast water habitat, slope, Number of trait states Significant Bêche & Statzner (2009)
elevation, precipitation
Stream Natural environmental variability Rao’s quadratic entropy Weak correlation Peru & Dolédec (2010)
Stream Local environmental variables Dendrogram-based Significant Colzani et al. (2013)
measure
Stream Local environmental variables Functional dispersion Significant Colzani et al. (2013)
Stream Glacial cover Rao’s quadratic entropy Significant Brown & Milner (2012)
Stream Glacial cover Dendrogram-based Significant Brown & Milner (2012)
measure
River floodplain turbidity, salinity, chlorophyll-a, Rao’a quadratic entropy Significant Gallardo et al. (2011)
organic nitrogen
Stream Size of the watershed Number of unique Significant Schmera et al. (2012)
combination of trait
states
Stream Stream width Combinatorial functional Weak correlation Podani et al. (2013)
diversity
Stream Natural watersheds Number of unique Significant Schmera et al. (2013)
combination of trait
states
Stream Wood conditioning Rao’s quadratic entropy Significant Vaz et al. (2014)

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Table 3 Case studies evaluating the response of functional diversity to human impact
Habitat Predictor variable Response variable Effect Reference

Stream Alien species Shannon diversity Sensitive Devin et al. (2005)

Stream Sewage pollution Rao’s quadratic entropy Sensitive Peru & Dolédec (2010)
Stream Environmental stressors Rao’s quadratic entropy No correlation Vandewalle et al. (2010)
River Sediment contamination Rao’s quadratic entropy Not sensitive Colas et al. (2011)
River Sediment contamination Rao’s quadratic entropy Not sensitive Colas et al. (2011)
Stream Nutrient enrichment, in- Number of unique Sensitive Schmera et al. (2012)
stream habitat combination of trait
degradation states
Stream Sediment accumulation Rao’s quadratic entropy Sensitive Buendia et al. (2013)
River Flow reduction Rao’s quadratic entropy Not sensitive Graeber et al. (2013)
Stream Stream regulation Rao’s quadratic entropy Sensitive Martinez et al. (2013)
Stream Hydromorphological Rao’s quadratic entropy Weak response Feld et al. (2014)
alteration
Lake Development of Rao’s quadratic entropy Sensitive Kovalenko et al. (2014)
watershed
Stream Fine sediment Rao’s quadratic entropy Sensitive Lange et al. (2014)
accumulation

(Townsend & Hildew, 1994), through their response native macroinvertebrate taxa in the Moselle River,
traits, and thus environmental filtering has an indirect and thus taxon richness did not change. In contrast,
effect on response traits, and this change modifies functional diversity of macroinvertebrates signifi-
functional diversity (Fig. 1). Interestingly, we did not cantly increased due to functional redundancy (taxon
find any study that examines how phylogenetic loss did not result in functional loss) and due to the
constrains influence the link between response and new functions provided by the invasive taxa.
effect traits. In contrast, in terrestrial ecology, Cadotte
et al. (2011) demonstrated that by comprising trait
variability across taxonomic levels, phylogenetic How functional diversity drives ecosystem
diversity could be a better predictor of ecosystem functions and which ones?
function than species diversity. Finally, we should
extend Fig. 1 by the note that abiotic factors might As the definition of functional diversity promises a
also have direct impact on ecosystem functions (i.e. link between biodiversity and ecosystem functions, we
temperature mediates multiple processes, Truchy examined which ecosystem functions were examined
et al., 2015). and how functional diversity of macroinvertebrates
Results regarding the sensitivity of functional drives these functions. Interestingly, none of the
diversity of macroinvertebrates to human impact are papers using a mathematically defined functional
contradictory (Table 3). Most of the studies have diversity measure specified or quantified any ecolog-
shown that functional diversity is sensitive to human ical functions.
impact. Despite the globally similar response of This finding is surprising, because experimental
functional diversity and species richness to human evidences suggest that the diversity of suspension
impacts, our review has detected differences as well. feeders influences the filtering of suspended particu-
These differences may stem from variation in anthro- late material from water (Cardinale et al., 2002) and
pogenic pressure, the selected functional diversity because the effects of detritivore diversity on leaf litter
measures, taxonomic resolution and taxon pools over processing has become a flagship of stream ecology
the study regions as well as from the existence of research (Jonsson & Malmqvist, 2000, 2003; Gessner
functional redundancy. For instance, Devin et al. et al., 2010; Lecerf & Richardson, 2010; Frainer et al.,
(2005) found that invasive species replaced some 2014; Frainer & McKie, 2015).

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Hydrobiologia (2017) 787:27–44 39

The most likely explanation is that the authors complex nature of functional diversity. For support-
using the term ‘‘functional diversity’’ were not inter- ing comparative analyses, we suggest to use already
ested in concrete ecological functions, and focused used indices for quantifying functional diversity of
only on aspects of diversity that influence ecosystem freshwater macroinvertebrates.
functions in general. For understanding this, we should
also keep in mind that macroinvertebrates play many Study autecology of macroinvertebrates
different functions in freshwater habitats. Conse-
quently, if a taxon list is not restricted to a single Our review showed that autecological information on
functional group (i.e. detritivores), then functional many species is often lacking. This missing knowl-
diversity cannot be connected to a single ecosystem edge clearly hampers the development of functional
function (i.e. detritus processing) only. This indicates diversity research. This also suggests that further
missing information on how functional diversity of autecological studies are needed.
entire macroinvertebrate assemblages can be linked to
ecosystem functions. Consequently, functional diver- Study the relationship between taxonomic
sity measured by several traits should be interpreted as resolution and functional diversity
a general indicator.
On the other hand, studies examining macroinver- Our review showed that the knowledge on the effect of
tebrate diversity—macroinvertebrate ecosystem func- taxonomic resolution on functional diversity is still in
tion relationships have never used the term infancy. As most of the studies use mixed taxonomic
‘‘functional diversity’’, only modelled biodiversity resolutions, our present state of knowledge might
through changes in species richness. This indicates strongly be influenced by the relationship between
that studying biodiversity through species richness taxonomic resolution and functional diversity. Exam-
might be more straightforward than through a multi- ining this relationship would result in a stronger
faceted term like functional diversity. support of our present state of knowledge.

Study functional diversity of freshwater

Recommendations for future research macroinvertebrates in underrepresented continents
and habitats
Incorporate phylogenetic relatedness of the taxa
in quantifying functional diversity We found that functional diversity research is biased
towards European and North American streams and
Although some functional diversity measures assume further studies are required in less examined conti-
the non-independence of traits, a direct incorporation nents (Africa, Asia, Australia and Oceania) and
of phylogenetic relatedness of taxa into the measure- habitats (ponds, lakes).
ment of functional diversity is still missing.
Narrow the gap between functional diversity
Use the same methodology research and research on biodiversity—ecosystem
functioning
Unfortunately, the limited number of replicated
studies did not allow us to draw solid and statisti- We found that functional diversity research does not
cally sound conclusions. In addition, the wide meet with ecosystem functions. This suggests that
variety of functional diversity measures with differ- knowledge on the impact of functional diversity on
ent mathematical properties prevented us from ecosystem processes is apparent, and functional
conducting a meta-analysis, which may weaken diversity of entire macroinvertebrate assemblages
our conclusions. However, although the use of a can be regarded as general indicator. Thus, in the
single functional diversity measure would support future, effort should be made to uncover the relation-
drawing general conclusions, it would at the same ship between functional diversity and ecosystem
time severely restrict the examination of the functions.

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40 Hydrobiologia (2017) 787:27–44

Conclusions Boersma, K. S., M. T. Bogan, B. A. Henrichs & D. A. Lytle,

2014. Invertebrate assemblages of pools in arid-land
streams have high functional redundancy and are resistant
Although theory suggests a direct link between to severe drying. Freshwater Biology 59: 491–501.
functional diversity and ecosystem functions, the Bonada, N., N. Prat, V. H. Resh & B. Statzner, 2006. Devel-
latter are rarely addressed in freshwater macroinver- opments in aquatic insect biomonitoring: a comparative
tebrate research. Consequently, freshwater ecologists analysis of recent approaches. Annual Review of Ento-
mology 51: 495–523.
quantify functional diversity as a general indicator, Botta-Dukát, Z., 2005. Rao’s quadratic entropy as a measure of
and little is known about the true functions of functional diversity based on multiple traits. Journal of
macroinvertebrates in freshwaters. We found that Vegetation Science 16(5): 533–540.
functional diversity of macroinvertebrates is sensitive Brown, L. E. & A. M. Milner, 2012. Rapid loss of glacial ice
reveals stream community assembly process. Global
to different environmental variables as well as to the Change Biology 18: 2195–2204.
different kinds of anthropogenic impact. Finally, Brouard, O., R. Cereghino, B. Corbara, C. Leroy, L. Pelozuelo,
several factors hinder drawing general conclusions A. Dejan & J. F. Carrias, 2012. Understorey environments
from the existing studies, including bias towards influence functional diversity in tank-bromeliad ecosys-
tems. Freshwater Biology 57: 815–823.
certain geographic regions and certain measures of Buendia, C., C. N. Gibbins, D. Verica, R. J. Batalla & A.
functional diversity. Douglas, 2013. Detecting the structural and functional
impacts of fine sediment on stream invertebrates. Ecolog-
Acknowledgments This research was supported by the ical Indicators 25: 184–196.
Hungarian Scientific Research Fund (OTKA K104279) and Cadotte, M. W., K. Carscadden & N. Mirotchnick, 2011.
the Academy of Finland. The last author benefited from funds of Beyond species:functional diversity and the maintenance
the European Community’s Seventh Framework Program, of ecological processes and services. Journal of Applied
Grant Agreement No. 603629-ENV-2013-6.2.1-Globaqua. Ecology 48: 1079–1087.
Cardinale, B. J., M. A. Palmer & S. L. Collins, 2002. Species
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