Science of the Total Environment 599–600 (2017) 1912–1921

Contents lists available at ScienceDirect

Science of the Total Environment

journal homepage: www.elsevier.com/locate/scitotenv

Temporal variability in taxonomic and trait compositions of invertebrate

assemblages in two climatic regions with contrasting flow regimes
Sylvain Dolédec a,⁎, Jessica Tilbian a, Núria Bonada b
a
UMR 5023, LEHNA, Biodiversité et Plasticité dans les Hydrosystèmes, Bât Forel RDC, 6 rue Raphaël Dubois, Université Lyon 1, 69100 Villeurbanne, France
b
Grup de Recerca Freshwater Ecology and Management (FEM), Departament de Biologia Evolutiva, Ecologia i Ciències Ambientals, Facultat de Biologia, Institut de Recerca de la Biodiversitat
(IRBio), Universitat de Barcelona (UB), Diagonal 643, 08028 Barcelona, Catalonia, Spain

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• Contrasting flow regimes in least-dis-

turbed rivers influences aquatic biodi-
versity.
• Taxonomy varies more in Mediterra-
nean intermittent than perennial tem-
perate rivers.
• Traits compositions and functional di-
versity vary less than taxonomic com-
positions.
• Higher richness in Mediterranean rivers
results in higher community specializa-
tion.
• Taxonomic and functional diversity re-
cover after drying events in intermittent
natural rivers.

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

Article history: Context: Understanding natural temporal changes in Mediterranean rivers with contrasting flow regimes in rela-
Received 9 April 2017 tion to those of temperate rivers may prove helpful in predicting effects of climate change on aquatic biodiversity.
Received in revised form 5 May 2017 Goal: We aimed to compare temporal variability in taxonomic and trait compositions of nearly natural rivers in
Accepted 5 May 2017 two climatic regions with varying flow regimes to address the effects of future climate changes on aquatic biodi-
Available online xxxx
versity in reference conditions.
Methods: We analysed taxonomic and biological trait compositions using the Foucard multivariate method to
Keywords:
Benthic invertebrates
compare within-site temporal variability levels and the evolution of within-date spatial variability patterns. In
Trait combinations addition, we assessed the effects of temporal variability levels on taxonomic and functional diversity and on com-
Foucard method munity specialization.
Mediterranean streams Results: Our results reveal (i) highly fluctuating environments of the Mediterranean region, particularly in inter-
Flow intermittence mittent rivers, which lead to higher levels of temporal variability in both taxonomic and trait compositions of
benthic invertebrate assemblages, with marked synchrony in Mediterranean streams linked to contrasting
flow characteristics; (ii) higher degrees of taxonomic richness associated with higher levels of functional diver-
sity in Mediterranean rivers relative to temperate rivers, (iii) higher temporal stability for functional diversity
and trait compositions of benthic invertebrate assemblages than for taxonomic richness and compositions;
and (iv) a recovery of all diversity metrics following drying events in intermittent sites.
Conclusion: This study offers insight into a rarely addressed question concerning the temporal variability of trait
compositions in benthic invertebrate assemblages among rivers differing in terms of flow regimes. It suggests
that temperate rivers will experience higher levels of temporal variability in terms of taxonomic and trait com-
positions under future climatic change scenarios, even in sites that will remain perennial, resulting in higher

⁎ Corresponding author.
E-mail address: sylvain.doledec@univ-lyon1.fr (S. Dolédec).

http://dx.doi.org/10.1016/j.scitotenv.2017.05.057
0048-9697/© 2017 Elsevier B.V. All rights reserved.
 S. Dolédec et al. / Science of the Total Environment 599–600 (2017) 1912–1921
levels of taxonomic and functional diversity. This lack of temporal stability in least-disturbed situations should be
taken into account when developing bioassessment tools based on reference conditions.
1. Introduction
The spatio-temporal variability of physical and chemical conditions
shapes the biological characteristics of running water. Temporal vari-
ability, and particularly seasonality, is known to influence temporal
changes in communities of different ecosystems (e.g. Tonkin et al. in
press). For river ecosystems, flow variability is a key driver of temporal
variability in aquatic assemblages (see e.g. Arthington et al., 2006). For
intermittent rivers and ephemeral streams (hereafter referred to as
IRESs, i.e. those for which flow conditions have ceased or those which
have dried up in time and space), flow variability patterns can greatly
affect the magnitude of the temporal variability of benthic invertebrate
assemblages (e.g. Bêche and Resh, 2007; Datry et al., 2014a, 2014b). In
contrast, compared to IRES and discarding inter-annual variability, the
temporal variability of benthic invertebrate assemblages in perennial
rivers is typically low (Scarsbrook, 2002). IRESs are commonly found
in many regions of the world, representing 59% of the streams in the
United States (Nadeau and Rains, 2007) and 43% of running water
drained in Greece (Tzoraki and Nikolaidis, 2007). In the current context
of climate change, many regions with IRESs should undergo increasing-
ly severe drying events, and few perennial rivers should evolve towards
intermittence (Döll and Schmied, 2012). The effects of drying on aquatic
assemblages, and particularly on benthic invertebrates, have attracted
more interest over the last decade (e.g. Leigh et al., 2016a).
It has been shown that differences in the taxonomic compositions of
benthic invertebrate assemblages could be exacerbated by drying
events when comparing wet and dry seasons (Bêche et al., 2006) or con-
trasting aquatic habitats (riffle-pools vs isolated pools) (e.g. Bonada et
al., 2006, 2007b; Bêche et al., 2009). Studies on functional responses to
drying events are now being more frequently conducted (e.g.
García-Roger et al., 2013; Cid et al., 2016; Leigh et al., 2016b; Vorste et
al., 2016a, 2016b), but we have yet little knowledge on the annual var-
iation of the trait composition of benthic invertebrate assemblages in
IRES.
Benthic invertebrates have adapted to IRESs by developing traits
that confer them with resistance or resilience to conditions of flow in-
termittence (Bonada et al., 2007a; Robson et al., 2011; Datry et al.,
2014a). For example, some species can survive and resist dry periods
by entering in diapause, whereas others can disperse and re-colonize
a river when flow resumes. In addition, organisms with short life cycles
and producing several generations in a year (multivoltinism) can com-
plete their life cycles before a drying period occurs and can maximize
the number of offspring reaching reproduction, in turn synchronizing
their life cycles with flow regimes (Lytle and Poff, 2004). In the Mediter-
ranean Basin, IRESs are common whereas in temperate regions, these
rivers are rarer (Bonada and Resh, 2013). Various projections on climat-
ic changes in Europe for 2050 predict an increase in the number of tem-
perate streams with Mediterranean characteristics along with high
temporal flow fluctuations and the potential drying out of all or parts
of streams (Arnell, 1999; Beniston et al., 2007). Based on this context,
an examination of current differences between assemblages of temper-
ate and Mediterranean rivers (perennial and IRES) could offer perspec-
tives on the future impacts of climate changes on running water and on
community responses to such changes in terms of temporal dynamics of
biodiversity levels and functioning.
In this paper, we use benthic macroinvertebrate samples collected
bimonthly over a year in perennial and IRES areas of two regions char-
acterized by contrasting climates (Mediterranean: Catalonia, Spain;
temperate: Jura, France) to test the following hypotheses on temporal
variations of assemblage structures (taxa compositions and diversity)
1913
© 2017 Elsevier B.V. All rights reserved.
and functions (trait compositions and diversity): (i) Mediterranean riv-
ers should be much more temporally variable in terms of structures and
functions than temperate rivers, as hydrological features are much more
variable within a year due to seasonal variations in precipitation and
temperature patterns (Bonada and Resh, 2013); (ii) such temporal var-
iability should be much more pronounced in intermittent than in peren-
nial rivers, as flow intermittence resets aquatic communities and is
considered to be a key process that constraints the structure and func-
tioning of IRESs (Leigh et al., 2016a), (iii) trait compositions should be
temporally more stable than taxonomic compositions linked to the po-
tential trait convergence of species of similar habitat variability (e.g.
Bêche et al., 2006); and (iv) the higher temporal variability of assem-
blage in Mediterranean rivers should involve a higher degree of func-
tional diversity.
2. Material and methods
2.1. Study area
Six stream sites situated in two climatic regions were sampled, in-
cluding two perennial sites in a temperate region (Jura, France) and
four sites in a Mediterranean region (Catalonia, Spain) (Table 1),
among which two perennial and two IRES sites were considered. For
each region and flow type, rivers were selected for having the most sim-
ilar natural physical and chemical characteristics based on current pub-
lic water agency information. Both the Cuisance and Doubs temperate
rivers are considered to be of good or very good ecological status
(http://sierm.eaurmc.fr/surveillance/eaux-superficielles/). All Mediter-
ranean rivers drain through natural parks (the Nespres and Talamanca
are located in the Sant Llorenç Natural Park, whereas the Algars and
Canaletes are located in the Els Ports Natural Park) and thus are consid-
ered to be of good or very good ecological status (http://aca-web.gencat.
cat/app/WDMA/wdma.jsp; http://iber.chebro.es/geoportal/).
2.2. Data
2.2.1. Fauna abundance
Bimonthly sampling was carried out at each site from May 2005 to
March 2006. For each sampling period and from each site, three random
“kick” samples were collected (kick of 2 mn per sample, mesh = 250 μm).
Samples were pooled and abundances were transformed into ln(x + 1)
to reduce effects of dominant species due to a heterogeneity of abun-
dances between the Mediterranean and temperate sites. Macroinverte-
brates (except Diptera) were identified at the genus level following
Tachet et al. (2010).
2.2.2. Biological traits
In total, 11 biological traits distributed across 59 categories defined
for European benthic invertebrate genera were extracted from existing
databases (Tachet et al., 2010; Statzner et al., 2007; Bonada et al., 2007a;
Bonada and Dolédec, 2011). These traits characterize their life cycles
(maximal size, life duration, number of generations per year, and aquat-
ic stages), resistance and resilience capacities (dispersal, locomotion
and substrate relations, and resistance forms), reproduction character-
istics, food types, feeding habits, and respiration types (see Appendix
1). In these databases, the affinity of benthic invertebrate genera to
each trait category is quantified via “fuzzy” coding (Chevenet et al.,
1994) by assigning a score varying from “0” (no affinity) to X (X, the
strongest affinity; X varies from 3 to 5 for locomotion and substrate re-
lations and for food, respectively). This method allows accounting for
1914 S. Dolédec et al. / Science of the Total Environment 599–600 (2017) 1912–1921
Table 1
Geographic characteristics and flow types of the six sites studied (TP for temperate perennial, MP for Mediterranean perennial and MI for Mediterranean intermittent).
Site code Region Flow type
TP1 Temperate Perennial
TP2 Temperate Perennial
MP1 Mediterranean Perennial
MP2 Mediterranean Perennial
MI1 Mediterranean Intermittent
MI2 Mediterranean Intermittent
the variability of species traits necessarily occurring within genera and
to standardize information from diverse sources. In addition to taxono-
my, the compositions of assemblages in terms of trait relative abun-
dances was examined by multiplying the frequencies of each category
per trait by the relative log-transformed abundances of species in a sam-
ple (see e.g. Gayraud et al., 2003; Schmera et al., 2014).
2.3. Data analyses
2.3.1. Multi-table analyses
We analysed temporal variability patterns for both regions and flow
regimes using Foucart's correspondence analysis (here abbreviated as
FCoa; Foucart, 1984; Pavoine et al., 2007). This multi-table technique in-
volves analysing K tables (e.g. one per site or one per month in our
study, K = 6 in both cases) sharing the same rows (e.g. sampling dates
or sites) and columns (taxa or traits). The FCoa involves using correspon-
dence analysis as a core analysis, implying that it analyses the relative
abundances of taxa (traits) and that each table has its own marginal
weighting (Pavoine et al., 2007). The FCoa is carried out over two steps.
First, through an inter-structure analysis (see e.g. Thioulouse and
Chessel, 1987), a reference table presenting average similarities across
all tables is established to show common (spatial or temporal) patterns
across tables. Using the notation of Pavoine et al. (2007), the reference
K
table is obtained by computing table Y ¼ ∑k¼1 α k Xk with weights
K
αk chosen so that ∑k¼1 α 2k ¼ 1 and given that they maximize the average
covariance among pairs of tables. An eigenanalysis is then performed on
the resulting reference table, yielding factorial axes that describe the
common or reference structure (temporal or spatial in our study) across
tables. Second, through an intra-structure analysis (Thioulouse and
Chessel, 1987), rows and columns of each individual table are projected
onto reference axes as supplementary individuals and supplementary
variables, respectively. This latter step allowed us to compare the tem-
poral variability of benthic invertebrate assemblages at each site and
their spatial variability across dates. We further computed the overall
temporal variability level for each site by summing eigenvalues
(representing variances) of the separate analyses performed for each
site (date). Finally, we assessed differences in temporal variability in
taxonomic and trait compositions across regions and flow types
through ANOVA tests. Post-hoc Tukey's HSD tests allowed us to evalu-
ate whether pairs of region and flow types differed significantly.
2.3.2. Abundance, richness, diversity and community specialization
We used the raw abundance to obtain the total number of individ-
uals collected at each site and in each month. We further addressed
richness and diversity levels of benthic invertebrate assemblages both
in terms of taxonomy and traits. Due to heterogeneities in the number
of individuals collected from sites on each sampling date, we corrected
genus richness levels using a rarefaction procedure (see Oksanen et al.,
2016). We thus randomly drew a fixed number of individuals (n = 149,
i.e. the minimum abundance found at any date and from any site) and
computed the rarefied richness level for each sample. For each sample,
we also computed the Simpson diversity value. Functional diversity
was assessed via Rao quadratic entropy (Champely and Chessel,
2002), which sums the trait distances of any pair of species in an assem-
blage weighted by their relative abundance. We computed trait
River name Latitude Longitude Altitude (m)
Cuisance 46°52′19.97″N 5°48′14.47″E 366
Doubs 46°52′19.97″N 6°12′29.27″E 981
Algars 40°51′10.83″N 0°15′16.99″E 551
Canaletes 40°57′12.79″N 0°21′53.99″E 420
Nespres 41°43′18.49″N 1°58′55.46″E 462
Talamanca 41°43′18.49″N 1°59′46.26″E 485
distances adapted to fuzzy coded variables following Pavoine et al.
(2009). Finally, we evaluated community specialization levels using in-
dices proposed by Mondy and Usseglio-Polatera (2014). This involves
computing a taxon specialization index (TSI) for each taxon and each
trait, with a high TSI value denoting taxon specialization for a given
trait. The community specialization index (CSI) was calculated for
each trait by averaging the individual TSIs of all taxa in an assemblage
weighted by the respective log-transformed abundances of taxa. Finally,
we used the average of CSI computed for each trait as an index of overall
community specialization. The magnitude of the five metrics (abun-
dance, rarefied richness, simpson diversity, Rao index and community
specialization) was tested against regional (Mediterranean vs. temper-
ate) and flow type differences using ANOVA and post-hoc Tukey's
HSD tests. We used a false discovery error correction to address prob-
lems associated with multiple comparison tests.
Statistics and graphical outputs were produced using the ade4 (Dray
and Dufour, 2007), vegan (Oksanen et al., 2016) and FD (Laliberté et al.,
2014) libraries available through the R freeware program (R Develop-
ment Core Team, 2016).
3. Results
3.1. Taxonomic composition
3.1.1. Within-site temporal variability
The first two axes of the FCoa performed on the six genera-by-dates
tables (one per site) accounted for 61% of total variance in the taxonomic
composition (38% for the first axis). Common temporal patterns separat-
ed the late autumn and winter (November and January with a large num-
ber of Crustacea) from early spring (March), late spring and summer
(May and July with a large number of Heteroptera) and autumnal transi-
tion (September) (Fig. 1A). In comparison to that of the temperate peren-
nial sites (TP), the temporal variability of the taxonomic composition was
found to be higher in the Mediterranean sites (MP for Mediterranean pe-
rennial sites and MI for Mediterranean intermittent sites) and particularly
in MI sites (Fig. 2A; Table 2A, ANOVA F2,29 = 13.73, P b 0.031 with Tukey's
HSD tests MI N MP, P b 0.035, MI N MP P b 0.05 and MP ≈ MI P N 0.82).
Higher temporal variability levels in the MI sites are mainly attributable
to different assemblages found in March (Fig. 4A).
3.1.2. Within-date temporal variability
The first two axes of the FCoa performed on the six genera-by-sites
tables (one per date) accounted for 64% of the total variance in the tax-
onomic composition (38% for the first axis). Common spatial patterns
show a clear difference between TP, MP and MI sites (Fig. 1B). Taxa be-
longing to Odonata, Coleoptera and Heteroptera (OCH) dominate the
Mediterranean sites (Fig. 1B), whereas Tricladida and Plecoptera are
more prominent in the TP sites. Taxonomic differences between the
sites remained generally consistent across the sampling dates (Fig. 2B
and Table 3A).
3.2. Trait composition
3.2.1. Within-site temporal variability
The first two axes of the FCoa performed on the six trait-by-date ta-
bles (one per site) accounted for 76% of the total variance in the trait
 S. Dolédec et al. / Science of the Total Environment 599–600 (2017) 1912–1921 1915

Fig. 1. Reference patterns of the taxonomic compositions of assemblages using first two FCoa axes and showing (A) the average level of temporal variability (a line links dates) and (B) the
average level of spatial variability (see Table 1 for acronyms for the sites). Dots denote the positions of taxa along each axis. A label for groups [using the five first letters: Coleo =
Coleoptera, Crust = Crustacea, Ephem = Ephemeroptera, Heter = Heteroptera, Mollus = Molluscs, Odona = Odonata, other = other insects (Diptera and Megaloptera), Pleco =
Plecoptera, Trich = Trichoptera and Tricl = Tricladida] is placed at the average score of taxa belonging to a given group.

composition (42% for the first axis). Common temporal patterns sepa-
rated the late spring and summer (May, July) from the early autumn
(September), with a transition occurring in the late autumn and winter
(November and January) (Fig. 3A). In March, assemblages involved a va-
riety of trait categories corresponding to individuals eating large preys
(including small vertebrates), laying free clutches or clutches in vegeta-
tion, burrowing, and eating dead animals or fine sediment dominated
assemblages. For May and July, prominent trait categories included indi-
viduals with temporary attachments to substrates, nymphs as aquatic
stages and filter feeding. For September, assemblages mainly included
individuals with cells that protect against desiccation as a resistance
form, ovoviviparity and aerial respiration. Both July and September as-
semblages shared individuals of small sizes and that exhibited cocoon
resistance and plastron respiration (Fig. 3A). Like the taxonomic compo-
sitions, trait compositions showed higher levels of temporal variability
in the Mediterranean sites, and especially the MI sites, relative to the
TP sites (Fig. 4A; Table 2B, ANOVA F2,29 = 18.06, P b 0.025 with
Tukey HSD's tests MI N MP P b 0.021, MI N MP P b 0.05 and MP ≈ MI P
N 0.40). Higher levels of temporal variability found in the MI sites
were mainly due to different trait compositions of assemblages found
in September (after drought) (Fig. 4A).
3.2.2. Within-date temporal variability
The first two axes of the FCoa performed on the six trait-by-site ta-
bles (one per) accounted for 78% of the total variance in the trait compo-
sition (50% for the first axis). Common spatial patterns separated the TP
sites from the Mediterranean sites (Fig. 3B). TP assemblages included
more individuals that lay free clutches, have cocoons for resistance pur-
poses, and consume fine sediment. MI assemblages included more indi-
viduals that consume large preys (including small vertebrates), possess
cells that protect against desiccation or egg laying in vegetation, per-
form aerial respiration, and swim along water surfaces. MP assemblages
included more individuals of small and large sizes that exhibit tempo-
rary or permanent attachment and are filter feeders or piercers (Fig.
3B). Trait composition differences between the sites remained globally
consistent across the sampling dates (Fig. 4B and Table 3B).

Fig. 2. (A) Sampling dates (abbreviated by their first three characters) used for each site (TP: temperate perennial; MP: Mediterranean perennial; MI: Mediterranean intermittent) shown
on the first two axes of the FCoa applied to the six genera-by-site tables. Within each site, a line links sampling dates. (B) Sampling sites per date (abbreviated based on their first three
characters by month and year) on the first two axes of the FCoa applied to the six genera-by-date tables. A shaded convex hull connects the sites. Note that MI1 and MI2 dried out in May
and July, respectively.
1916 S. Dolédec et al. / Science of the Total Environment 599–600 (2017) 1912–1921

Table 2
Overall temporal within-site variance for (A) taxa and (B) trait compositions of inverte-
brate assemblages.
Sites (A)
MI1 3.166
MI2 4.976
MP1a 0.998
MP2a 0.788
TP1a 0.599
TP2a 0.280
a
Values were weighted according to the number of sampling dates in each site since
intermittent sites had two samples less than perennial.
3.3. Abundance, richness, diversity and community specialization
Temporal patterns in total abundance levels at the MI sites involved
progressive recovery after a drying period. Overall, perennial sites pre-
sented low abundances during September–November (Fig. 5A). No
temporal patterns appeared in terms of rarefied richness levels in TP,
whereas temporal variability was found in the Mediterranean sites
(Fig. 5B). Richness levels recovered after drying in MI sites to up to
values similar to those of MP sites, and especially for MI1. MP sites pre-
sented higher levels of richness from May–July than during the other
sampling periods. With the exceptional levels found for the MI sites,
functional diversity, Simpson diversity and community specialization
levels remained remarkably stable over time (Fig. 5C–E). Total abun-
dance levels were significantly higher in the temperate sites than in
the Mediterranean sites. The reverse pattern was found for all four
other metrics and especially for rarefied richness and Rao diversity
levels (Table 4).
4. Discussion
Overall, our results generally support our four hypotheses. First, the
structures and functions of Mediterranean river benthic invertebrate as-
semblages were found to be more temporally variable than those of
temperate rivers. Second, structural and functional temporal variability
levels were found to be more pronounced in intermittent rivers than in
perennial rivers. Third, the temporal variability of trait compositions
was found to be less important than that of the taxonomic compositions
of assemblages. Fourth, higher levels of temporal variability found in
Mediterranean river assemblages than those of temperate rivers im-
plied the presence of higher levels of taxonomic and trait diversity.
Resh, 2013). Together with spatial variability, temporal variability and
seasonality in particular forms the basis of population and community
patterns found in aquatic ecosystems worldwide (Cid et al., 2017). In
(B) addition to Mediterranean regions, other seasonal ecosystems exhibit
0.055 very high annual variability in benthic invertebrate compositions. Mon-
0.041 soonal regions, for example, present strong differences between wet
0.021 and dry seasons in different regions of the world (Jacobsen and
0.019
Encalada, 1998; Brewin et al., 2000; Bogan and Lytle, 2007; Mesa,
0.013
0.007 2012). The Mediterranean sites considered in our study also present ex-
pected community fluctuations over time when considering both taxo-
nomic and trait compositions. Sites located in temperate regions, with
less pronounced seasonal dynamics in respect to hydrological regime
maintain more uniform communities throughout the year, especially
in those regions with low predictability of hydrological events (Tonkin
et al. in press). In terms of structures, in agreement with our study
and studies performed in other Mediterranean and arid regions, Medi-
terranean rivers include higher proportions of lentic-like species, such
as Odonata, Coleoptera and Heteroptera, due to a dominance of pools
forming during the summer as a result of flow decline (Bonada et al.,
2006, 2007b; Bogan and Lytle, 2007). In contrast, higher proportions
of Ephemeroptera, Plecoptera and Trichoptera are known to be related
to lower temperatures, riffle dominance (Haidekker and Hering, 2008;
Bonada et al., 2012) and streamflow characteristics (Konrad et al.,
2008), explaining higher proportions of Plecoptera found in the temper-
ate rivers examined. Tricladida were exclusively found in the temperate
rivers due to their sensitivities to water temperatures and drought
(Durance and Ormerod, 2010).
Despite the differences identified between Mediterranean and tem-
perate rivers, we also found common temporal patterns between both
river types for specific taxa and traits. This suggests that temporal envi-
ronmental filters are stronger than regional environmental filters for
some benthic invertebrates. For example, in our study, Crustacea and
traits adapted to high flows and low temperatures (i.e. organisms per-
manently attached and eggs as resistance forms) dominated in the win-
ter and spring, whereas Heteroptera and traits adapted to low flows and
higher temperatures (i.e. organisms temporarily attached, aerial respi-
ration, and ovoviviparity) were generally prominent in the summer.
This pattern is clearly linked to current biological knowledge on flow re-
quirements associated with holobiotic vs. amphibiotic taxa and to re-
ductions in flows and increases in temperature occurring during the
summer relative to those of the winter found in the studied streams
(e.g. Bonada et al., 2007b; Statzner and Bêche, 2010; Tachet et al., 2010).
4.2. Temporal variability in intermittent vs. perennial rivers

4.1. Temporal variability in Mediterranean vs. temperate rivers Temporal variability levels were found to be higher in the intermit-
tent sites than in the perennial sites. Community changes between the
Temporal variability levels in benthic invertebrate taxonomic and wet and dry seasons are also known to be more significant for intermit-
trait compositions were found to be significantly higher for the Mediter- tent rivers than perennial rivers in other Mediterranean climate regions
ranean rivers than for the temperate rivers. In comparison to temperate of the world (e.g. California) (Bêche et al., 2006). Flow intermittence im-
rivers, Mediterranean rivers are characterized by high levels of seasonal poses a strong filter on aquatic assemblages, selecting taxa with partic-
variability in flow regimes, even for those rivers that maintain perennial ular traits (e.g. Bonada et al., 2007a; Datry et al., 2014a). Drought resets
flow conditions in the summer (Bêche and Resh, 2007; Bonada and aquatic assemblages, and during flow resumption, riverbeds are colo-
nized by resilient or resistant taxa (Leigh et al., 2016b). Assemblages
in IRESs are thus subjected to higher levels of temporal environmental
Table 3
Overall spatial within-date variance for (A) taxa and (B) trait compositions of invertebrate
heterogeneity that result in higher levels of temporal turnover for
assemblages. aquatic and terrestrial organisms colonizing dry riverbeds (Corti and
Datry, 2016). In terms of functions, in our study, Mediterranean inter-
Dates (A) (B)
mittent rivers were characterized by a dominance of species with traits
Januarya 1.663 0.056 adapted to resist and recover from summer drying, whereas Mediterra-
Marcha 2.165 0.051
nean perennial rivers exhibited trait compositions similar to those of
May 1.670 0.068
July 1.806 0.074 temperate rivers (see also Bonada et al., 2007a). With few exceptions
Septembera 2.263 0.065 (e.g. Bêche et al., 2009; Mouthon and Daufresne, 2006), the recovery
Novembera 1.654 0.054 of aquatic assemblages after drying has frequently been observed in
a
Values were weighted according to the number of sampling dates in each site since IRESs (e.g. Boulton, 2003; Lake, 2003; Vorste et al., 2016a). This capacity
intermittent sites had two samples less than perennial. for assemblages to quickly regain their pre-drought compositions is
 S. Dolédec et al. / Science of the Total Environment 599–600 (2017) 1912–1921 1917

Fig. 3. Reference patterns of the trait compositions of assemblages using first two FCoa axes and showing (A) the average level of temporal variability (a line linking dates) and (B) the
average level of spatial variability. Trait categories showing the highest levels of variance on either axis are shown. Dots denote the positioning of other trait categories (see Appendix 1 for
acronyms of trait categories).

explained by the presence of refuges in hyporheic zone (Datry, 2012),
which allows benthic invertebrates to survive in the sediments of
dried rivers pending the return of flow to recolonize habitats (Brock et
al., 2003; Stubbington et al., 2016). While this benthic invertebrate
“seedbank” can be critical for recolonization after flow resumption, in
Mediterranean climate rivers, resilience also plays a major role in ben-
thic invertebrate recovery (Leigh et al., 2016b). In our case, resilient
traits, such as small sizes, multivoltine life cycles and aerial dispersal
patterns, and resistance traits, such as egg laying in terrestrial habitats
or in vegetation or diapauses, were found to be significantly more prev-
alent in MI sites than in MP sites.
The spring and late summer periods presented the highest levels of
taxonomic and trait variability in the MI sites, respectively. In most MI
sites, riffles cease and lentic-like species colonize lentic habitats during
the spring when drought conditions start to manifest, maximizing tax-
onomic differences as drying advances. Differences in taxonomic com-
positions are thus maximized when comparing wet and dry periods,
as has been shown for many aquatic organisms (Cid et al., 2016). The
start of the dry season also influences temporal trajectories of benthic
invertebrate assemblages, as many species life cycles are synchronized
with the dry period (e.g. López-Rodríguez et al., 2009). In contrast to
the observed taxonomic temporal patterns, trait compositions especial-
ly differed at the end of the summer in MI sites, corresponding to the
rewetting period. This suggests that MI sites are characterized by
species with traits adapted to flow intermittence regardless of the peri-
od. This trait composition shifts during the rewetting period, a critical
moment at which point benthic invertebrate assemblages reappear
once again and when resilient traits typically dominate (Leigh et al.,
2016b).
4.3. Temporal stability of biological trait compositions
Overall, differences between the sites were consistent across the
study period in terms of taxonomic and trait compositions, denoting
the importance of regional variables in the structure and functioning
of assemblages (Grenouillet et al., 2001). However, according to FCoa
ordinations, the temporal variability of trait compositions appeared to
be much lower than that of taxonomic compositions by a factor of 3,
in agreement with our third hypothesis. Stream environmental condi-
tions are viewed as a strong abiotic filter (i.e. physical severity) that
sieves appropriate biological traits (Poff, 1997) to yield high levels of re-
gional stability in trait compositions of assemblages (e.g. Statzner et al.,
2001, 2004). Such high levels of temporal stability in trait compositions
of Mediterranean climate assemblages follow from the findings of Bêche
et al. (2006), who found that dry and wet seasons are more similar in
terms of traits than in terms of taxonomic compositions. Such stability
in trait convergence appears to apply to other aquatic organisms (see
e.g. Lamouroux et al., 2002; Villeger et al., 2013).

Fig. 4. (A) Sampling dates (abbreviated by their first three characters) for each site (TP: temperate perennial; MP: Mediterranean perennial; MI: Mediterranean intermittent) on the first
two axes of the FCoa applied to the six trait-by-site tables. For each site, a line links sampling dates. (B) Sampling sites per date (abbreviated by the first three characters of a month) on the
first two axes of the FCoa applied to the six trait-by-date tables. A shaded convex hull links the sites. Note that MI1 and MI2 dried out in May and July, respectively.
1918 S. Dolédec et al. / Science of the Total Environment 599–600 (2017) 1912–1921

Fig. 5. Temporal changes in (A) abundance, (B) rarefied richness, (C) taxonomic diversity measured by the Simpson index, (D) functional diversity measured by Rao quadratic entropy and
(E) community specialization measured by the CSI index for each site (see acronyms of sites in Table 1).

4.4. Consequences for richness and functional diversity levels
While taxonomic and trait compositions of assemblages differ be-
tween seasons overall when comparing perennial and intermittent riv-
ers in Mediterranean regions (e.g. Bêche et al., 2006; Hershkovitz and
Gasith, 2013; García-Roger et al., 2013; but see Sánchez-Montoya et
al., 2009), taxonomic richness levels are typically similar between sea-
sons in both types of rivers (Bêche et al., 2006; Sánchez-Montoya et
al., 2009; but see Bonada et al., 2007b). Our results do follow this pat-
tern, as all diversity metrics in intermittent Mediterranean rivers quick-
ly recover to values similar to those found in perennial Mediterranean
rivers (Fig. 5). In agreement with our fourth hypothesis, a higher level
of functional diversity was found to be associated with higher levels of
temporal variability in assemblages of Mediterranean rivers compared
to temperate ones, suggesting that Mediterranean taxa may perform
more diverse functional roles than temperate taxa. As indicated above,
traits such as cells that protect against desiccation, egg clutches in veg-
etation, small and large sizes, temporarily and permanently attached or-
ganisms, and swimmers have been deemed resilient traits by several
authors (Bonada et al., 2007a; Robson et al., 2011; Datry et al., 2014a)
and were largely found in the Mediterranean rivers examined in our
study. Accordingly, richness levels were found to be higher in the Med-
iterranean rivers than in the temperate ones (e.g. Bonada et al., 2007a),
which in turn have influenced community specialization patterns, i.e.
Mediterranean assemblages include more specialist taxa, whereas tem-
perate streams include more generalist taxa. Ecological specialization is
known to decrease competition between species (e.g. Devictor et al.,
2010). In addition, total abundance decreases with ecological specializa-
tion, suggesting that Mediterranean genera tend to use more marginal
habitats than temperate genera. Such a decrease in abundance with spe-
cialization seems a common pattern described elsewhere (see e.g.
Statzner et al., 2008) but rather new for invertebrate assemblages.
4.5. Climate change and management implications
Climate change is expected to have dramatic effects on organisms
and ecosystems, including changes in their distribution ranges and phe-
nologies (e.g. Walther et al., 2002; Parmesan, 2006). For benthic inver-
tebrates, model projections suggest that the distribution of most
species will be reduced and that their climatically suitable areas will

Table 4
Mean values and standard deviations (in parentheses) for the selected metrics describing abundance, rarefied richness, taxonomic and functional diversity and specialization of assem-
blages (CSI index) by region and flow type. Probability values of corresponding ANOVA and Tukey's HSD tests for multiple comparisons are given (TP for temperate perennial, MP for Med-
iterranean perennial and MI for Mediterranean intermittent).

TP MP MI F2,29 P Tukey's HSD

Abundance 7939 (±6983) 978 (±652) 396 (±269) 10.4 0.0004 MI ≈ MP N TP

Rarefied richness 12 (±3) 19 (±5) 18 (±4) 9.8 0.0006 MI ≈ MP N TP
Simpson index 0.939 (±0.014) 0.953 (±0.008) 0.933 (±0.022) 4.9 0.0150 MP N MI ≈ TP
Rao index 0.164 (±0.010) 0.196 (±0.012) 0.201 (±0.010) 37.2 0.0000 MI ≈ MP N TP
CSI 0.49 (±0.00) 0.53 (±0.16) 0.50 (±0.17) 26.1 0.0000 MI ≈ MP N TP
 S. Dolédec et al. / Science of the Total Environment 599–600 (2017) 1912–1921
drift northward and eastward in Europe, dramatically reducing the
number of species in southern and central Europe (Domisch et al.,
2013; Markovic et al., 2014). In addition, several studies have shown
that benthic invertebrates are advancing their life cycles and are evolv-
ing from uni- to multi-voltinism (e.g. Hassall et al., 2007; Filipe et al.,
2013), indicating that climate change will also affect the temporal vari-
ability of invertebrate assemblages. Our spatio-temporal study shows
that future benthic invertebrate assemblages found in temperate re-
gions will experience higher levels of temporal variability in taxonomic
and trait compositions, which will involve an increase in functional di-
versity. The assumption supporting this is that Mediterranean taxa
will shift to temperate regions in the near future. Species distribution
models show this trend overall (see references above), though these
models do not account for biological interactions between shifting spe-
cies and local ones, which decreases model reliability. Many Mediterra-
nean species, especially those adapted to high flow variability levels,
exhibit strong dispersal abilities and are expected to arrive in temperate
areas in the coming decades (Bonada et al., 2007a; García-Roger et al.,
2013). For example, the Odonata species Trithemis annulata, originally
distributed across northern Africa, has quickly expanded its distribution
area to southern Mediterranean France over the last 20 years (Grand,
1994) and to northern temperate Spain over the last 30 years (Ayres
et al., 2007). Benthic invertebrates in central Europe are more general-
ists in terms of niche requirements than those of southern Europe
(our study; Hering et al., 2009), suggesting that they will be better
able to cope with climate change. Therefore, uncertainties remain re-
garding whether temporal variations in community compositions will
result from adaptations to climate change of local species (i.e. changes
in their life cycle characteristics) or from the arrival and establishment
of new species.
The number of watercourses undergoing drying is expected to in-
crease in several regions of the world and even outside of Mediterra-
nean climate regions. For temperate Europe, the few existing
projections of flow regime shifts suggest that this region will also
show an increase in its number of intermittent rivers (Döll and
Schmied, 2012). Snelder et al. (2013), for example, suggested that the
probability of intermittence in France is expected to increase by 2–3%
if summer air temperature increases by 1 °C or if mean annual rainfall
decreases by 100 mm. The presence of more intermittent rivers alters
network connectivity levels and jeopardizes the persistence of aquatic
organisms (Jaeger et al., 2014). Our results show that invertebrate as-
semblages under these new flow regime conditions will experience
more temporal variability than those in perennial flows, amplifying
the effects of climate change. Species distribution models for aquatic or-
ganisms in temperate Europe should thus also include predictor vari-
ables that consider sensitivities to flow intermittence, most likely in a
way similar to the manner in which dispersal abilities are currently con-
sidered (e.g. see Markovic et al., 2014).
5. Concluding remarks
Our analysis of the temporal variability of benthic invertebrates in
temperate vs. Mediterranean regions shows that much consideration
should be devoted to temporal patterns of aquatic assemblages for
stream management in temperate regions. When temporal variability
levels are so high that benthic invertebrate assemblages extend beyond
the limits of a reference or least-disturbed state, the reliability of bioas-
sessments can be altered (Milner et al., 2016). Therefore, the temporal
variability of natural conditions should be more seriously considered
through bioassessment tools to disentangle natural temporal patterns
from the effects of human disturbances and thus properly assess de-
grees of biota alteration (Linke et al., 1999). This is especially relevant
in IRES where the use of EPT-based bioassessment tools cannot be ap-
propriate throughout the year. As IRES are part of the landscapes of
Mediterranean regions, applied research in these areas has largely fo-
cused on developing new tools and methodologies that reliably assess
1919
the ecological status of these rivers under the Water Framework Direc-
tive (see Cid et al., 2017). Data obtained on these highly temporally var-
iable rivers should serve as a benchmark for the successful management
and conservation agendas for temperate rivers applied according to fu-
ture climate change scenarios.
Supplementary data to this article can be found online at http://dx.
doi.org/10.1016/j.scitotenv.2017.05.057.
Acknowledgements
Funding: The first author has been supported by the European Union
7th Framework Programme Funding under Grant agreement no.
603629-ENV-2013-6.2.1-Globaqua.
We thank Cesc Múrria for his assistance in the field. We also thank
the two anonymous reviewers who contributed to improving this pa-
per. This article was edited for proper English language, grammar, punc-
tuation, spelling and overall style by two highly qualified native English-
speaking editors at American Journal Experts (certification verification
key: A8B9-2BFE-C55A-6513-A2FC).
References
Arnell, N.W., 1999. The effect of climate change on hydrological regimes in Europe: a con-
tinental perspective. Glob. Environ. Chang. 9:5–23. http://dx.doi.org/10.1016/S0959-
3780(98)00015-6.
Arthington, A.H., Bunn, S.E., Poff, N.L., Naiman, R.J., 2006. The challenge of providing envi-
ronmental flow rules to sustain river ecosystems. Ecol. Appl. 16:1311–1318. http://
dx.doi.org/10.1890/10510761(2006)016[1311:TCOPEF]2.0.CO;2.
Ayres, C., González, I., Lorenzo, O., Cordero, A., 2007. Nuevas citas de Trithemis annulata
(Palisot de Beauvois, 1807) (Odonata: Libellulidae) en Galicia. Boletín de la Sociedad
Entomológica Aragonesa 41, 402.
Bêche, L.A., Resh, V.H., 2007. Short-term climatic trends affect the temporal variability of
macroinvertebrates in California Mediterranean streams. Freshw. Biol. 52:
2317–2339. http://dx.doi.org/10.1111/j.1365-2427.2007.01859.x.
Bêche, L., McElravy, E.P., Resh, V.H., 2006. Long-term seasonal variation in the biological
traits of benthic macroinvertebrates in two Mediterranean- climate streams in Cali-
fornia, U.S.A. Freshw. Biol. 51:56–75. http://dx.doi.org/10.1111/j.1365-2427.2005.
01473.x.
Bêche, L.A., Connors, P.G., Resh, V.H., Merenlender, A.M., 2009. Resilience of fishes and in-
vertebrates to prolonged drought in two California streams. Ecography 32:778–788.
http://dx.doi.org/10.1111/j.1600-0587.2009.05612.x.
Beniston, M., Stephenson, B., Christensen, O.B., Ferro, C.A.T., Frei, C., Goyette, S., Halsnaes,
K., Holt, T., Jylhä, K., Koffi, B., Palutikof, J., Schöll, R., Semmler, T., 2007. Future extreme
events in European climate: an exploration of regional climate model projections.
Clim. Chang. 81:71–95. http://dx.doi.org/10.1007/s10584-006-9226-z.
Bogan, M.T., Lytle, D.A., 2007. Seasonal flow variation allows ‘time-sharing’ bydisparate
aquatic insect communities in montane desert streams. Freshw. Biol. 44:290–304.
http://dx.doi.org/10.1111/j.1365-2427.2006.01691.x.
Bonada, N., Dolédec, S., 2011. Do Mediterranean genera not included in Tachet et al. 2002
have Mediterranean trait characteristics? Limnetica 30, 129–141.
Bonada, N., Resh, V.H., 2013. Mediterranean-climate streams and rivers: geographically
separated but ecological comparable freshwater systems. Hydrobiologia 719:1–29.
http://dx.doi.org/10.1007/s10750-013-1634-2.
Bonada, N., Rieradevall, M., Prat, N., Resh, V.H., 2006. Benthic macroinvertebrate assem-
blages and macrohabitat connectivity in Mediterranean-climate streams of northern
California. J. N. Am. Benthol. Soc. 25:32–43. http://dx.doi.org/10.1899/0887-
3593(2006)25[32:BMAAMC]2.0.CO;2.
Bonada, N., Dolédec, S., Statzner, B., 2007a. Taxonomic and biological trait differences of
stream macroinvertebrate communities between Mediterranean and temperate re-
gions: implications for future climatic scenarios. Glob. Chang. Biol. 13:1658–1671.
http://dx.doi.org/10.1111/j.1365-2486.2007.01375.x.
Bonada, N., Rieradevall, M., Prat, N., 2007b. Macroinvertebrate community structure and
biological traits related to flow permanence in a Mediterranean river network.
Hydrobiologia 589:91–106. http://dx.doi.org/10.1007/s10750-007-0723-5.
Bonada, N., Dolédec, S., Statzner, B., 2012. Spatial autocorrelation patterns of stream inver-
tebrates: exogenous and endogenous factors. J. Biogeogr. 39:56–68. http://dx.doi.org/
10.1111/j.1365-2699.2011.02562.x.
Boulton, A.J., 2003. Parallels and contrasts in the effects of drought on stream macroinver-
tebrate assemblages. Freshw. Biol. 48:1173–1185. http://dx.doi.org/10.1046/j.1365-
2427.2003.01084.x.
Brewin, P.A., Buckton, S.T., Ormerod, S.J., 2000. The seasonal dynamics and persistence of
stream macroinvertebrates in Nepal: do monsoon floods represent disturbance?
Freshw. Biol. 44:581–594. http://dx.doi.org/10.1046/j.1365-2427.2000.00608.x.
Brock, M.A., Nielsen, D.L., Shiel, R.J., Green, J.D., Langley, J.D., 2003. Drought and aquatic
community resilience: the role of eggs and seeds in sediments of temporary wet-
lands. Freshw. Biol. 48:1207–1218. http://dx.doi.org/10.1046/j.1365-2427.2003.
01083.x.
Champely, S., Chessel, D., 2002. Measuring biological diversity using Euclidean metrics.
Environ. Ecol. Stat. 9:167–177. http://dx.doi.org/10.1023/A:1015170104476.
1920 S. Dolédec et al. / Science of the Total Environment 599–600 (2017) 1912–1921
Chevenet, F., Dolédec, S., Chessel, D., 1994. A fuzzy coding approach for the analysis of
long-term ecological data. Freshw. Biol. 31:295–309. http://dx.doi.org/10.1111/j.
1365-2427.1994.tb01742.x.
Cid, N., Verkaik, I., García-Roger, E.M., Rieradevall, M., Bonada, N., Sanchez-Montoya, M.M.,
Gomez, R., Suarez, M.L., Vidal-Abarca, M.R., Demartini, D., Buffagni, A., Erba, S.,
Karazouas, I., Skoulikidis, N., Prat, N., 2016. A biological tool to assess flow connectiv-
ity in reference temporary streams from the Mediterranean Basin. Sci. Total Environ.
540:178–190. http://dx.doi.org/10.1016/j.scitotenv2015.06.086.
Cid, N., Bonada, N., Carlson, S.M., Grantham, T.E., Gasith, A., Resh, V.H., 2017. High variabil-
ity is a defining component of Mediterranean-climate rivers and their biota. Water 9:
1–24. http://dx.doi.org/10.3390/w9010052.
Core Team, R., 2016. R: A Language and Environment for Statistical Computing. R Founda-
tion for Statistical Computing, Vienna, Austria.
Corti, R., Datry, T., 2016. Terrestrial and aquatic invertebrates in the riverbed of an inter-
mittent river: parallels and contrasts in community organisation. Freshw. Biol. 61:
1308–1320. http://dx.doi.org/10.1111/fwb.12692.
Datry, T., 2012. Benthic and hyporheic invertebrate assemblages along a flow intermit-
tence gradient: effects of duration of dry events. Freshw. Biol. 57:563–574. http://
dx.doi.org/10.1111/j.1365-2427.2011.02725.x.
Datry, T., Larned, S.T., Tockner, K., 2014a. Intermittent rivers: a challenge for freshwater
ecology. Bioscience 64:229–235. http://dx.doi.org/10.1093/biosci/bit027.
Datry, T., Larned, S.T., Fritz, K.M., Bogan, M.T., Wood, P.J., Meyer, E.I., Santos, A.N., 2014b.
Broad-scale patterns of invertebrate richness and community composition in tempo-
rary rivers: effects of flow intermittence. Ecography 37:94–104. http://dx.doi.org/10.
1111/j.1600-0587.2013.00287.x.
Devictor, V., Clavel, J., Julliard, R., Lavergne, S., Mouillot, D., Thuiller, W., Venail, P., Villéger,
S., Mouquet, N., 2010. Defining and measuring ecological specialization. J. Appl. Ecol.
47:15–25 http://doi.org/10.1111/j.1365-2664.2009.01744.x.
Döll, P., Schmied, H.M., 2012. How is the impact of climate change on river flow regimes
related to the impact on mean annual runoff? A global-scale analysis. Environ. Res.
Lett. 7:14–37. http://dx.doi.org/10.1088/1748-9326/7/1/014037.
Domisch, S., Araújo, M.B., Bonada, N., Pauls, S.U., Jähnig, S.C., Haase, P., 2013. Modelling
distribution in European stream macroinvertebrates under future climates. Glob.
Chang. Biol. 19:752–762. http://dx.doi.org/10.1111/gcb.12107.
Dray, S., Dufour, A.B., 2007. The ade4 package: implementing the duality diagram for ecol-
ogists. J. Stat. Softw. 22, 1–20.
Durance, I., Ormerod, S.J., 2010. Evidence for the role of climate in the local extinction of a
cool-water triclad. J. N. Am. Benthol. Soc. 29:1367–1378. http://dx.doi.org/10.1899/
09-159.1.
Filipe, A.F., Lawrence, J.E., Bonada, N., 2013. Vulnerability of stream biota to climate
change in mediterranean climate regions: a synthesis of ecological responses and
conservation challenges. Hydrobiologia 719:331–351. http://dx.doi.org/10.1007/
s10750-012-1244-4.
Foucart, T., 1984. Analyse Factorielle de Tableaux Multiples. Masson, Paris.
García-Roger, E.M., Sánchez-Montoya, M.M., Cid, N., Erba, S., Karazouas, I., Verkaik, I.,
Rieradevall, M., Gómez, R., Suárez, M.L., Vida-Abarca, M.R., Demartini, D., Buffagni,
A., Skoulikidis, N., Bonada, N., Prat, N., 2013. Spatial scale effects on taxonomic and bi-
ological trait diversity of aquatic macroinvertebrates in Mediterranean streams.
Fundam. Appl. Limnol. 183:89–105. http://dx.doi.org/10.1127/1863-9135/2013/
0429.
Gayraud, S., Statzner, B., Bady, P., Haybach, A., Scholl, F., Usseglio-Polatera, P., Bacchi, M.,
2003. Invertebrate traits for the biomonitoring of large European rivers: an initial as-
sessment of alternative metrics. Freshw. Biol. 48:2045–2064. http://dx.doi.org/10.
1046/j.1365-2427.2003.01139.x.
Grand, D., 1994. Sur Trithemis annulata (Palisot de Beauvais, 1805) en France continentale
et en Espagne du nord-est (Odonata, Anisoptera: Libellulidae). Martinia 10, 65–71.
Grenouillet, G., Hugueny, B., Carrel, G.A., Olivier, J.M., Pont, D., 2001. Large-scale synchro-
ny and inter-annual variability in roach recruitment in the Rhône River: the relative
role of climatic factors and density-dependent processes. Freshw. Biol. 46:11–26.
http://dx.doi.org/10.1046/j.1365-2427.2001.00637.x.
Haidekker, A., Hering, D., 2008. Relationship between benthic insects (Ephemeroptera,
Plecoptera, Coleoptera, Trichoptera) and temperature in small and medium-sized
streams in Germany: a multivariate study. Aquat. Ecol. 42:463–481. http://dx.doi.
org/10.1007/s10452-007-9097-z.
Hassall, C., Thompson, D.J., French, G.C., Harvey, I.F., 2007. Historical changes in the phe-
nology of British Odonata are related to climate. Glob. Chang. Biol. 13:933–941.
http://dx.doi.org/10.1111/j.1365-2486.2007.01318.x.
Hering, D., Schmidt-Kloiber, A., Murphy, J., Lücke, S., Zamora-Muñoz, C., López-Rodríguez,
M.J., Huber, T., Graf, W., 2009. Potential impact of climate change on aquatic insects: a
sensitivity analysis for European caddisflies (Trichoptera) based on distribution pat-
terns and ecological preferences. Aquat. Sci. 71:3–14. http://dx.doi.org/10.1007/
s00027-009-9159-5.
Hershkovitz, Y., Gasith, A., 2013. Resistance, resilience, and community dynamics in med-
iterranean-climate streams. Hydrobiologia 719:59–75. http://dx.doi.org/10.1007/
s10750-012-1387-3.
Jacobsen, D., Encalada, A., 1998. The macroinvertebrate fauna of Ecuatorian highland
streams and the influence of wet and dry seasons. Arch. Hydrobiol. 142, 53–70.
Jaeger, K.L., Olden, J.D., Pelland, N.A., 2014. Climate change poised to threaten hydrologic
connectivity and endemic fishes in dryland streams. Proc. Natl. Acad. Sci. U. S. A. 111:
13894–13899. http://dx.doi.org/10.1073/pnas.1320890111.
Konrad, C.P., Brasher, A.M.D., May, J.T., 2008. Assessing streamflow characteristics as lim-
iting factors on benthic invertebrate assemblages in streams across the western Unit-
ed States. Freshw. Biol. 53:1983–1998. http://dx.doi.org/10.1111/j.1365-2427.2008.
02024.x.
Lake, P.S., 2003. Ecological effects of perturbation by drought in flowing waters. Freshw.
Biol. 48:1161–1172. http://dx.doi.org/10.1046/j.1365-2427.2003.01086.x.
Laliberté, E., Legendre, P., Shipley, B., 2014. FD: measuring functional diversity from mul-
tiple traits, and other tools for functional ecology. R Package Version 1.0-12.
Lamouroux, N., Poff, N.L., Angermeier, P.L., 2002. Intercontinental convergence of stream
fish community traits along geomorphic and hydraulic gradient. Ecology 83:
1792–1807. http://dx.doi.org/10.1890/0012-9658(2002)083[1792:ICOSFC]2.0.CO;2.
Leigh, C., Boulton, A.J., Courtwright, J.L., Fritz, K., May, C.L., Walker, R.H., Datry, T., 2016a.
Ecological research and management of intermittent rivers: an historical review
and future directions. Freshw. Biol. 61:1181–1199. http://dx.doi.org/10.1111/fwb.
12646.
Leigh, C., Bonada, N., Boulton, A.J., Hugueny, B., Larned, S.T., Vander, Vorste R., Datry, T.,
2016b. Invertebrate assemblage responses and the dual roles of resistance and resil-
ience to drying in intermittent rivers. Aquat. Sci. 78:291–301. http://dx.doi.org/10.
1007/s00027-015-0427-2.
Linke, S., Bailey, R.C., Schwindt, J., 1999. Temporal variability of stream bioassessments
using benthic macroinvertebrates. Freshw. Biol. 42:575–584. http://dx.doi.org/10.
1046/j.1365-2427.1999.00492.x.
López-Rodríguez, M.J., de Figueroa, J.M.T., Fenoglio, S., Bo, T., Alba-Tercedor, J., 2009. Life
strategies of 3 Perlodidae species (Plecoptera) in a Mediterranean seasonal stream
in southern Europe. J. N. Am. Benthol. Soc. 28:611–625. http://dx.doi.org/10.1899/
08-105.1.
Lytle, D.A., Poff, N.L., 2004. Adaptation to natural flow regimes. TREE 19:94–100. http://dx.
doi.org/10.1016/j.tree.2003.10.002.
Markovic, D., Carrizo, S., Freyhof, J., Cid, N., Lengyel, S., Scholz, M., Kasperdius, H., Darwall,
W., 2014. Europe's freshwater biodiversity under climate change; distribution shifts
and conservation needs. Divers. Distrib. 20:1097–1107. http://dx.doi.org/10.1111/
ddi.12232.
Mesa, L.M., 2012. Interannual and seasonal variability of macroinvertebrates in monsoon-
al climate streams. Braz. Arch. Biol. Technol. 55, 403–410.
Milner, A.M., Woodward, A., Freilich, J.E., Black, R.W., Resh, V.H., 2016. Detecting signifi-
cant change in stream benthic macroinvertebrate communities in wilderness areas.
Ecol. Indic. 60:524–537. http://dx.doi.org/10.1016/j.ecolind.2015.07.025.
Mondy, C.P., Usseglio-Polatera, P., 2014. Using fuzzy-coded traits to elucidate the non-
random role of anthropogenic stress in the functional homogenisation of invertebrate
assemblages. Freshw. Biol. 59:584–600. http://dx.doi.org/10.1111/fwb.12289.
Mouthon, J., Daufresne, M., 2006. Effects of the 2003 heatwave and climatic warming on
mollusk communities of the Saône: a large lowland river and of its two main tribu-
taries (France). Glob. Chang. Biol. 12:441–449. http://dx.doi.org/10.1111/j.1365-
2486.2006.01095.x.
Nadeau, T.L., Rains, M.C., 2007. Hydrological connectivity between headwater streams
and downstream waters: how science can inform policy? J. Am. Water Resour.
Assoc. 43:118–133. http://dx.doi.org/10.1111/j.1752-1688.2007.00010.x.
Oksanen, J., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R., O'Hara, R.B., Simpson, G.L.,
Solymos, P., Stevens, M.H.H., Wagner, H., 2016. Vegan: community ecology package.
R package version 2.3-5. https://CRAN.R-project.org/package=vegan.
Parmesan, C., 2006. Ecological and evolutionary responses to recent climate change.
Annu. Rev. Ecol. Evol. Syst. 37:637–669. http://dx.doi.org/10.1146/annurev.ecolsys.
37.091305.110100.
Pavoine, S., Blondel, J., Baguette, M., Chessel, D., 2007. A new technique for ordering asym-
metrical three-dimensional data sets in ecology. Ecology 88:512–523. http://dx.doi.
org/10.1890/05-1806.
Pavoine, S., Vallet, J., Dufour, A.B., Gachet, S., Daniel, H., 2009. On the challenge of treating
various types of variables: application for improving the measurement of functional
diversity. Oikos 118:391–402. http://dx.doi.org/10.1111/j.1600-0706.2008.16668.x.
Poff, N.L., 1997. Landscape filters and species traits: towards mechanistic understanding
and prediction in stream ecology. J. N. Am. Benthol. Soc. 16:391–409. http://dx.doi.
org/10.2307/1468026.
Robson, B., Chester, E., Austin, C., 2011. Why life history information matters: drought ref-
uges and macroinvertebrate persistence in non-perennial streams subject to a drier
climate. Mar. Freshw. Res. 62:801–810. http://dx.doi.org/10.1071/MF10062.
Sánchez-Montoya, M.M., Suárez, M.L., Vidal-Abarca, M.R., 2009. Seasonal and interannual
variability of macroinvertebrate reference communities and its influence on bioas-
sessment in different Mediterranean stream types. Fundam. Appl. Limnol. 174:
353–367. http://dx.doi.org/10.1127/1863-9135/2009/0174-0353.
Scarsbrook, M.R., 2002. Persistence and stability of lotic invertebrate communities in New
Zealand. Freshw. Biol. 47:417–431. http://dx.doi.org/10.1046/j.1365-2427.2002.00810.x.
Schmera, D., Podani, J., Eros, T., Heino, J., 2014. Combining taxon-by-trait and taxon-by-
site matrices for analysing trait patterns of macroinvertebrate communities: a rejoin-
der to Monaghan & Soares (2014). Freshw. Biol. 59:1551–1557. http://dx.doi.org/10.
1111/fwb.12369.
Snelder, T.H., Datry, T., Lamouroux, N., Larned, S.T., Sauquet, E., Pella, H., Catalogne, C.,
2013. Regionalization of patterns of flow intermittence from gauging station records.
Hydrol. Earth Syst. Sci. 17:2685–2699. http://dx.doi.org/10.5194/hess-17-2685-2013.
Statzner, B., Bêche, L.A., 2010. Can biological invertebrate traits resolve effects of multiple
stressors on running water ecosystems? Freshw. Biol. 55:80–119. http://dx.doi.org/
10.1111/j.1365-2427.2009.02369.x.
Statzner, B., Bis, B., Dolédec, S., Usseglio-Polatera, P., 2001. Perspectives for biomonitoring
at large spatial scales: a unified measure for the functional composition of inverte-
brate communities in European running waters. Basic Appl. Ecol. 2:73–85. http://
dx.doi.org/10.1078/1439-1791-00039.
Statzner, B., Dolédec, S., Hugueny, B., 2004. Biological trait composition of European
stream invertebrate communities: assessing the effects of various trait filter types.
Ecography 27:470–488. http://dx.doi.org/10.1111/j.0906-7590.2004.03836.x.
Statzner, B., Bonada, N., Dolédec, S., 2007. Conservation of taxonomic and biological trait
diversity of European stream macroinvertebrate communities: a case for a collective
public database. Biodivers. Conserv. 16:3609–3632. http://dx.doi.org/10.1007/
s10531-007-9150-1.
 S. Dolédec et al. / Science of the Total Environment 599–600 (2017) 1912–1921
Statzner, B., Bonada, N., Dolédec, S., 2008. Predicting the abundance of European stream
macroinvertebrates using biological attributes. Oecologia 156 (1):65–73. http://dx.
doi.org/10.1007/s00442-008-0972-7.
Stubbington, R., Gunn, J., Little, S., Worrall, T.P., Wood, P.J., 2016. Macroinvertebrate
seedbank composition in relation to antecedent duration of drying and multiple
wet-dry cycles in a temporary stream. Freshw. Biol. 61:1293–1307. http://dx.doi.
org/10.1111/fwb.12770.
Tachet, H., Richoux, P., Bournaud, M., Usseglio-Polatera, P., 2010. Invertébrés d'eau Douce:
Systématique, Biologie, Écologie. third ed. CNRS éditions, Paris.
Thioulouse, J., Chessel, D., 1987. Les analyses multitableaux en écologie factorielle. I. De la
typologie d'état à la typologie de fonctionnement par l'analyse triadique. Acta Oecol.
Oecol. Gen. 8, 463–480.
Tonkin, J.D., Bogan, M.T., Bonada, N., Rios-Touma, B., Lytle, D.A., 2017. Seasonality and pre-
dictability shape temporal species diversity. Ecology http://dx.doi.org/10.1002/ecy.
1761 (in press).
Tzoraki, O., Nikolaidis, N.P., 2007. A generalized framework for modeling the hydrologic
and biogeochemical response of a Mediterranean temporary river basin. J. Hydrol.
346:112–121. http://dx.doi.org/10.1016/j.jhydrol.2007.08.025.
1921
Villeger, S., Grenouillet, G., Brosse, S., 2013. Decomposing functional-diversity reveals that
low functional-diversity is driven by low functional turnover in European fish assem-
blages. Glob. Ecol. Biogeogr. 22:671–681. http://dx.doi.org/10.1111/geb.12021.
Vorste, R.V., Corti, R., Sagouis, A., Datry, T., 2016a. Invertebrate communities in gravel-bed,
braided rivers are highly resilient to flow intermittence. Freshw. Sci. 35:164–177.
http://dx.doi.org/10.1086/683274.
Vorste, R.V., Malard, F., Datry, T., 2016b. Is drift the primary process promoting the resil-
ience of river invertebrate communities? A manipulative field experiment in an inter-
mittent alluvial river. Freshw. Biol. 61:1276–1292. http://dx.doi.org/10.1111/fwb.
12658.
Walther, G.R., Post, E., Convey, P., Menzel, A., Parmesan, C., Beebee, T.J.C., Fromentin, J.M.,
Hoegh-Guldberg, O., Bairlein, F., 2002. Ecological responses to recent climate change.
Nature 416:389–395. http://dx.doi.org/10.1038/416389a.