Ecology of Freshwater Fish 2014 Ó 2014 John Wiley & Sons A/S.

Ó 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

ECOLOGY OF
FRESHWATER FISH

Environmental and spatial processes: what

controls the functional structure of fish
assemblages in tropical rivers and headwater
streams?
Rodrigo A. Carvalho1, Francisco L. Tejerina-Garro2
1
Departamento de Ecologia, Programa de P
os-graduacß~ao em Ecologia e Evolucß~ao, Universidade Federal de Goi
as, Instituto de Ci^encias Biol
ogicas, Rodovia
Goi^ania-Ner

opolis km 5, Campus II Itatiaia, Goi^ania, 74001-970, GO Brasil
2
Centro de Biologia Aqu
atica, Pontif
ıcia Universidade Cat
olica de Goi
as – Campus II, Av. Engler s/n, Jardim Mariliza, Goi^ania, 74605-010, GO Brasil

Accepted for publication April 27, 2014

Abstract – In this study, we investigated functional structure patterns of tropical headwater and river fish
assemblages. We hypothesised that environmental conditions are primarily structuring headwater streams leading to
functionally clustered assemblages, whereas processes that favour functional overdispersion would guide river
assemblages. For 27 headwater streams and 22 rivers, we used eight functional traits for calculating two functional
indexes: mean pairwise distance (MPD) and net relatedness index (NRI). We performed linear regressions between
indexes and species richness, a multiple regression between NRI and eight environmental variables and a variation
partitioning to disentangle the role of environment and space on NRI. Our findings indicate that fish assemblages of
headwaters are structured by environmental conditions as most assemblages in this habitat displayed a tendency to
clustering and MPD/NRI were not correlated with species diversity, whereas the opposite pattern was observed for
river habitat. Four environmental variables (channel depth, water velocity, dissolved oxygen and turbidity) explain
56% of functional structure variation. These variables seem to function as selective filters in headwaters, whereas
channel depth may be determinant for functional overdispersion of river fish assemblages. Components associated
with space are also influencing the functional structure. Limitations of species dispersal through space (between
both habitat types) appear as a possible cause to this. In this sense, both environmental conditions and processes
linked with space are capable of influencing the functional structure of tropical headwater streams and river fish
assemblages.

Key words: Central Brazil; mean pairwise distance; net relatedness index; Tocantins-Araguaia basin; variation partitioning

independent of their traits and/or interactions, would

Introduction
A central issue of ecological research relies on under-
standing which processes underlie the diversity pat-
terns of biological communities. A wide range of
explanations has been proposed to explain these pat-
terns in aquatic systems, including abiotic factors
(Poff & Allan 1995; Peres-Neto 2004; Hoeinghaus
et al. 2007; S

uarez et al. 2007) and biotic interactions
among species (Winston 1995; Taylor 1996, 1997).
The co-occurrence of species and their persistence,
be another possibility as proposed by the neutral the-
ory of Hubbell (2001). It has been demonstrated that
all three processes may act at the same time (Helmus
et al. 2007) or sequentially – in the case of environ-
mental gradients – to determine diversity patterns
(Mason et al. 2007). Therefore, the current challenge
no longer seems to be finding a valid mechanism but
comprehending which one most strongly influences
on local community organisation (Mouchet et al.
2010). For freshwater fish assemblages, some studies

Correspondence: Rodrigo A. Carvalho, Departamento de Ecologia, Universidade Federal de Goi
as – UFG, Caixa Postal 131, CEP, Goi^ania 74001-970, GO, Brasil.
E-mail: rodrigoassiscarvalho@gmail.com

doi: 10.1111/eff.12152 1
Carvalho & Tejerina-Garro
investigated such mechanisms and different findings
have been presented. Poff & Allan (1995) found that
the presence of fish species with generalist or specialist
feeding strategies is directly associated with hydrologi-
cal variability of streams. Peres-Neto (2004) showed
that habitat features are of greater importance for deter-
mining species co-occurrence than species interactions.
On the other hand, Winston (1995) demonstrated that
competition is a powerful force in determining species
co-existence and Gilliam & Fraser (2001) found out
that predation threat is capable of influencing the
movement of fish species along streams.
Traditionally, environmental conditions have been
used to explain the variation of diversity patterns in
biological communities (Sharma et al. 2011). The
role of environmental filters on freshwater fish
assemblages was explored by Smith & Powell (1971)
who proposed the filter model, which was later modi-
fied to include species traits (Poff 1997). According
to this model, fish species from the regional pool
must pass through a series of environmental filters to
establish themselves locally (Tonn et al. 1990).
Therefore, species from a local fish assemblage are
expected to respond similarly to environmental fac-
tors and probably share many traits (Mouillot et al.
2007). In this context, environmental filters can be
determinant factors in driving the composition of
local fish assemblages.
Despite the role of environment in structuring fish
assemblages, ecologists have found evidence that the
spatial structure of fish assemblages is also a result of
spatial patterns. Sharma et al. (2011) found out that
assemblage composition of native and non-native fish
species in temperate lakes is driven by different eco-
logical rules. While native fish assemblages are struc-
tured by environmental conditions suggesting
environmental filtering, non-native fish assemblages
are structured by human-mediated dispersal. Assess-
ing the role of environmental and spatial components
through the use of variation partitioning (Borcard
et al. 1992; Peres-Neto & Legendre 2010) combined
with spatial statistical techniques [Moran’s Eigenvec-
tors Maps (MEM) Dray et al. 2006; Asymmetric
Eigenvectors Maps (AEM) Blanchet et al. 2008] is
now recognised as a key step for understanding the
ecological processes that rule community composi-
tion patterns.
In freshwater systems, headwater streams can be
considered as the most upstream areas in a river sys-
tem, and they are generally classified from first order
up to third order (Vannote et al. 1980). Abiotic fac-
tors in headwaters – such as water velocity, substrate
type, dissolved oxygen, water temperature and trans-
port of particulate organic matter (Poff 1997) – may
predominate over biotic interactions in structuring
local fish assemblages (Ostrand & Wilde 2002;
2
Grenouillet et al. 2004). Due to high variability in
their environment, these low-order streams frequently
support low-diversity and less-structured assemblages
(Jackson et al. 2001) and a few hardy species tend to
persist (Rahel & Hubert 1991). On the other hand,
there is an increase in habitat diversity and environ-
mental stability further downstream along fluvial gra-
dients (Meffe & Minkley 1987; Jackson et al. 2001).
This fact frequently allows the persistence of fish
assemblages with a higher number of species (Mat-
thews 1986). Given the potential influence of abiotic
factors as selective filters at headwater streams and
the higher stability of downstream areas (high-order
rivers), it is possible to derive predictions about the
functional structure of fish assemblages in these habi-
tat types. In headwater streams, where environmental
filtering seems to be more preponderant, and fish
assemblages are composed of few hardy species, we
expect the coexistence of functionally similar species
(functional clustering). By contrast, we may expect
the coexistence of more functionally dissimilar spe-
cies (functional overdispersion) in downstream areas,
where the environment is more stable and diverse,
and fish assemblages tend to be richer.
In this study, we used a set of tropical headwater
streams and rivers to understand functional diversity
and functional structure patterns of their fish assem-
blages, trying to elucidate which ecological processes
drive their functional structure patterns. First, we
investigated how the functional diversity and the
functional structure of fish assemblages are related to
species diversity in both habitat types (headwater
streams and rivers). After that, we evaluated how the
variation of fish assemblages’ functional structure is
related to different environmental variables. Finally,
we explored the variation of fish assemblages’ func-
tional structure between headwater streams and riv-
ers. We hypothesise that headwater streams are
primarily structured by environmental variables, lead-
ing to functionally clustered assemblages, whereas
rivers would be less influenced by the environment
and would be structured by processes that favour the
existence of functionally overdispersed assemblages,
such as competition or species dispersal ability. Here,
we tested how much of the variation in the functional
structure of fish assemblages is explained by multiple
components, namely environment, spatially structured
environment and space. This kind of approach allows
us to identify which processes are more likely to
structure fish assemblages, as the spatial component
and the spatially structured environment variation are
assumed to express the importance of neutral dynam-
ics (Gilbert & Lechowicz 2004). On the other side,
the environmental component may express the occur-
rence of important niche-based processes, such as
environmental filtering.

Material and methods
Study area
We conducted our study in the Tocantins-Araguaia
River Basin (hereafter called Tocantins-Araguaia
Basin) that drains Goi
as State territory, Central Bra-
zil. The Tocantins-Araguaia Basin has a drainage
area of approximately 767,000 km2 with a mean
annual discharge of 11,000 m³
s 1 (Costa et al.
2003). It has a well-defined dry season that occurs
between May and October and also a wet season that
extends between November and April (Albrecht &
Pellegrini-Caramaschi 2003; Quesada et al. 2004). In
this region, the knowledge about aquatic communities
and its biodiversity is still very incipient (Tejerina-
Garro 2008).
Data and sampling protocol
In this paper, we used a data set relative to 27 head-
water streams and 22 rivers located in the Tocantins-
Araguaia Basin (Fig. 1) at an average altitude of 450
and 390 m, respectively. We defined a headwater
stream by its location in the river system, order
(1st–3rd order; Vannote et al. 1980) and drainage
area (10 < drainage area < 1000 km²; Meybeck
et al. 1996). We defined a watercourse as a river
by its location in the river system, order (4th–6th
order) and drainage area (1000 < drainage area <
100,000 km2; Meybeck et al. 1996). We determined
headwater stream and river orders using Strahler’s
Fig. 1. Spatial distribution of headwater streams (circles) and rivers (triangles) sampled in the upper section of the Tocantins-Araguaia
River Basin, Central Brazil. The Tocantins-Araguaia basin is represented in the small map.
Functional structure of rivers and streams
modification of Horton’s scale (Petts 1994), and we
checked it using a geographical information system
map (1:250,000) available on the website of the
Sistema Estadual de Estat
ıstica e de Informacß~ ao
Geogr
afica de Goi
as (SIEG 2013).
All headwater streams and rivers were sampled
during the dry season when the flows are low and
fishes are captured more efficiently (Pease et al.
2012). Furthermore, the relationship between fish
assemblages’ structure and habitat structure in dry
season is stronger (Willis et al. 2005). All samplings
were conducted between May and September 2008,
and the location of the sites was defined according to
the possibility of access. Sampling locations were
marked with an equipment of Global Position System
(GPS; Garmin 12).
Fish species from headwater streams were sampled
with a seine net (4 m 9 1.5 m 9 1 cm of mesh
between opposing knots), while species from rivers
were collected with gillnets of different sizes of
opposing knots (10 m 9 1.5 m 9 12–70 mm).
Seine nets are an efficient sampling technique for col-
lecting fish fauna when the focus is on ecological
patterns of species richness and composition (Medei-
ros et al. 2010), but the presence of rocks and woody
debris in the bottom substrate, as found in rivers,
often limits the application of this method for captur-
ing fish species (Tejerina-Garro & M
erona 2000).
These authors indicate also that the use of different
mesh size of gillnets in repeated batteries is a useful
method that gives a reliable picture from the fraction
of the fish community sampled in rivers.
3
Carvalho & Tejerina-Garro
For each headwater stream, a reach of 50 m was
defined following Imhof et al. (1996), and the sam-
pling effort was two persons per 50 m per 10 foot-
steps. For rivers, the reach size was delimited as
1000 m. All specimens collected were stored in iden-
tified plastic bags and were put in plastic drums with
formaldehyde 10%. The specimens were separated
and identified using taxonomic keys and expert opin-
ion. Finally, specimens were stored in alcohol 70% at
the Aquatic Biology Center of the Pontif
ıcia
Universidade Cat
olica de Goi
as and the Laboratory
of Ichthyology of the Museum of Pontif
ıcia Univer-
sidade Cat
olica do Rio Grande do Sul.
Data matrices
To perform the analyses in this paper, we used four
data matrices. First, we constructed a presence–
absence matrix (species vs. local sites) and a func-
tional traits matrix (species vs. traits). Although we
had species abundance, this kind of data can be rela-
tively sensitive to different sampling techniques and
effort (Poff & Allan 1995). Therefore, to avoid any
bias generated by different sampling techniques used
in headwater and river habitats, we did not include
abundance data in our analyses. We used eight traits
to construct our functional traits matrix: average body
mass, trophic guild, water column position, parental
care, foraging location, substrate preference, foraging
method and migration (Tables S1 and S2). Body mass
was obtained directly from collected fish specimens,
and it was calculated as the average body mass found
for all specimens of the species collected. Trophic
guild was determined according to information pres-
ent in Melo (2011). This author identified the main
component of diet for each species and then classified
it in one of the following categories: algivorous,
omnivorous, carnivorous, herbivorous, detritivorous,
invertivorous and iliophagous. For species without
information in Melo (2011), we searched for the main
component of species’ diet using an online database
(FishBase; Froese & Pauly 2014) and specialised liter-
ature. Data for parental care, water column position,
foraging method and migration were taken from spec-
ialised literature and an online database for fishes
(FishBase; Froese & Pauly 2014; see Table S1 for
more details of traits categories). To determine sub-
strate preference, we looked for all locations where
the species were collected and identified local sub-
strate(s). Then, in the species traits matrix, we marked
all substrates where the species has occurred. Forag-
ing location was determined according to water velo-
city. Watercourses with water velocity > 20 cm
s 1
were considered as running waters (riffles and runs),
while those under this limit were considered as stand-
ing waters or slower pools (see Rezende 2007). When
4
we were not able to find information for a species, we
extrapolated the data for genus or family level when-
ever it was possible. If extrapolation was not possible
(a single species in the genus), species trait was con-
sidered as not available (NA).
Afterwards, we constructed an environmental vari-
ables matrix (local sites vs. environmental variables)
with altitude (m), channel depth (m), water velocity
(cm
s 1), channel width (m), turbidity (NTU),
dissolved oxygen (mg
l 1), pH, conductivity
(lS
cm 1) and water temperature (°C). In each reach,
three transversal transects were delimited where each
environmental variable could be measured. Altitude
was measured only in the first transect with a GPS
(Garmin 12). In all transects, the following variables
were measured: channel width with a proper device
to measure the distance (Bushnell Yardage Pro 500,
Bushnell Company, Lenexa, KS, USA, for large riv-
ers), dissolved oxygen and temperature with an oxi-
meter (Lutron YK-22DO, Lutron Eletronic Entreprise
Co., Ltd., Taipei, Taiwan), pH with a pH meter
(Lutron PH-208, Lutron Eletronic Enterprise Co.,
Ltd., Taipei, Taiwan), conductivity with a conductiv-
ity meter (WTW 315i, Xylem Group, White Plains,
NY, USA), water velocity with a flowmeter (Flow-
meter Model 2030, General Oceanics Inc., Miami,
FL, USA) and channel depth with a measuring rope.
Turbidity was measured only in the middle transect
of headwater streams and all transects of rivers, both
with a digital turbidimeter (LaMotte 2020, LaMotte
Company, Cherstertown, MD, USA). Each variable
was measured in one location inside the transect.
Finally, we constructed a site-by-edge matrix (local
vs. link edges) that indicates the links among sites
according to a directional processes (for more details
see Blanchet et al. 2008). We built our sites-by-edges
matrix according to the direction of the flow
(upstream–downstream) and considering that this
flow direction is used by fish species for larval dis-
persion (Agostinho et al. 2007).
Analyses
For each fish assemblage, we calculated an index of
functional diversity using the mean pairwise distance
(henceforth MPD, Webb et al. 2002). Despite its
usual use in the calculation of phylogenetic diversity,
a phylogeny and a functional dendrogram have simi-
lar structures and properties (Pavoine & Bonsall
2010); therefore, this measure can be used to calcu-
late functional diversity substituting the phylogenetic
distance matrix by a functional distance matrix (Kem-
bel et al. 2010; Pavoine & Bonsall 2010). Then, for
calculating functional diversity using MPD, we
substituted the phylogenetic distance matrix by a
functional distance matrix in the analysis (Kembel

et al. 2010; Pavoine & Bonsall 2010) and used the
following protocol: (i) conversion of species traits
matrix to a distance matrix, (ii) clustering distance
matrix into a functional dendrogram, (iii) transform-
ing the functional dendrogram into a phylogeny, that
is, converting it into an object with phylogenetic
properties, (iv) extracting distance matrix (‘cophenet-
ic matrix’) and (v) calculating functional diversity as
a measure of mean functional distances among all
taxa that occur in a sample. We obtained the distance
matrix using a modification of Gower’s distance as
we had both qualitative and quantitative traits
together (Pavoine et al. 2009) and the functional den-
drogram using the unweighted pair group method
with arithmetic averages (UPGMA) as the clustering
method.
For each fish assemblage, we also calculated an
index of community functional structure using the net
relatedness index (henceforth NRI; Webb 2000;
Webb et al. 2002). The NRI quantifies the distribu-
tion of taxa in a sample relative to a species pool
(Webb 2000) and gives the standardised effect of the
observed distances among species (Kembel &
Hubbell 2006). The NRI for each locality can be
measured as 1[(MPD MPDnull)/SDMPDnull ], where
the MPD is the observed mean pairwise distance
among species in the locality, MPDnull is the mean
MPD for that locality in 999 null communities and
SDMPDnull is the standard deviation of MPD for that
locality in 999 null communities (Webb et al. 2002).
This index is calculated by measuring the mean dis-
tance of each species to all other species in the same
community. Positive NRI values (P < 0.05) indicate
that co-occurring species in a community are more
functionally similar than expected by chance (func-
tional clustering), while negative values (P > 0.95)
point to species less functionally similar than
expected (Kembel & Hubbell 2006).
To obtain the NRI, we used the functional traits
matrix to calculate a distance matrix with a modifica-
tion of Gower’s distance (Pavoine et al. 2009) and
UPGMA to develop the functional dendrogram. Here,
we used the same approach for MPD to convert the
functional dendrogram into a phylogeny and extract
the ‘cophenetic’ matrix. Based on the ‘cophenetic’
matrix, we utilised the function ses.mpd (Kembel
et al. 2010) available in R software (R Core Team
2013) to create a series of null communities for each
fish assemblage. Then, the observed degree of clus-
tering was compared with those expected by chance.
We generated a set of 999 null communities for
each fish assemblage using the independent swap
algorithm (Gotelli & Entsminger 2001). This algo-
rithm randomises the community data matrix main-
taining constant species occurrence frequency and
species richness of each community. In the end, each
Functional structure of rivers and streams
null community has a NRI value, and all 999 values
will be used to create a null distribution of NRI val-
ues expected at random. Then, the observed NRI
value can be compared with the null distribution. We
considered as our regional pool the set of fish species
found in all rivers and streams sampled.
We performed two simple linear regressions for
each habitat type to examine the relationship of spe-
cies diversity with functional diversity and commu-
nity functional structure: (i) species richness versus
MPD and (ii) species richness versus NRI. MPD and
NRI were considered as response variables, while S
was the predictor variable. All analyses were per-
formed in the R software (R Core Team 2013).
We performed a multiple linear regression between
NRI and environmental variables to explore whether
environmental features are predicting the variation in
the functional structure among sites. We used a for-
ward stepwise selection of the environmental vari-
ables to reduce the cases of co-linearity (Oberdorff
et al. 1995). We ran the multiple linear regression in
R software (R Core Team 2013).
To test the contribution of the environment and
space for NRI variation, we performed a variation
partitioning analysis (Borcard et al. 1992; Peres-Neto
& Legendre 2010) using spatial descriptors and envi-
ronmental variables matrices as predictors and the
NRI values as our response variable. To obtain the
spatial descriptors, we used the AEM method pro-
posed by Blanchet et al. (2008). It takes into account
the distance among watercourses and the direction of
the flow to represent dispersal patterns among sam-
pled sites. Based on our sites-by-edges matrix and
the spatial coordinates of sampled sites, we created a
connexion diagram linking the sites to one another
according to the asymmetric processes influencing
our response variable. Then, the connexion diagram
was used to calculate the spatial descriptors. Given
the different nature and scales of our environmental
variables, we performed a log-transformation to
increase linearity and avoid extreme values (Sharma
et al. 2011), excepting for pH values.
When a single variable is used as a predictor, the
partition of the variance is based on a linear regres-
sion, and it uses the adjusted R2 to estimate the
unique and combined effects of environmental and
spatial predictors (Borcard et al. 1992; Peres-Neto &
Legendre 2010). The adjusted R2 values are capable
to provide unbiased estimates on the real contribution
of explanatory variables to the response variable (Oh-
tani 2000; Peres-Neto et al. 2006). All these analyses
were performed in R environment (R Core Team
2013) using AEM package for Asymmetric Eigen-
vectors Maps (Blanchet & Legendre 2013) and var-
part function present in vegan package for partition
analysis (Oksanen et al. 2013).
5
Carvalho & Tejerina-Garro
Results
Fish assemblages from headwater streams and riv-
ers contained 150 fish species. Of these, 121 spe-
cies were found in rivers and 72 in headwater
streams. Thirty-one species occurred only in rivers,
while 12 species only in headwater streams. The
mean average of species per local site was 11.75
species considering both rivers and headwater
streams. Taking into account only rivers, the mean
average of species per local site was 14, while the
mean average for headwater streams was 9.9 spe-
cies per local site.
The spatial patterns of functional grouping found
in this study showed that most rivers evaluated had
negative NRI values (18 out of 22), whereas most of
headwater streams (25 out of 27) had positive NRI
values (Fig. 2 and Table S3). According to our null
model, eight of the 22 rivers (36.4%) presented a sig-
nificant functional grouping (P < 0.05), and six of
them (27.3%) had fish assemblages with functional
overdispersion and two (9.1%) with functional clus-
tering (Table S3). On the other hand, 10 of the 27
headwater streams (34.5%) presented a significant
functional grouping (P < 0.05), with functional clus-
tering of fish assemblages (Table S3).
For rivers, linear regressions showed that S is not
correlated with MPD (Fig. 3a; adjusted R2 = 0.30,
P = 0.16), but it is negatively correlated with NRI
(Fig. 3b; adjusted R2 = 0.48, P = 0.02). This nega-
tive association shows that patterns of functional
Fig. 2. Spatial pattern of the NRI values of headwater streams (circles) and rivers (triangles) sampled in the Tocantins-Araguaia basin. Col-
ours of the circles and triangles correspond to significant (grey) and nonsignificant (white) cases of functional grouping at a 0.05 level
under the null model.
6
overdispersion (lower NRI values) of river fish
assemblages are partially explained (48%) by an
increase in species richness suggesting that functional
patterns in this habitat type may also be associated
with other factors. For headwater streams, linear
regressions indicated that S is not significantly corre-
lated with MPD (Fig. 3c; adjusted R2 = 0.23,
P = 0.22) or NRI (Fig. 3d; adjusted R2 = 0.20,
P = 0.30).
The multiple regression demonstrated that environ-
mental variables explain 56% of the total variation in
NRI values (Table 1; adjusted R2 = 0.56,
P = 0.0001). Based on the forward stepwise selec-
tion, four environmental variables were indicated as
influencing NRI variation: channel depth, water
velocity, dissolved oxygen and turbidity (Table 1).
Variation partitioning revealed that neither the
local environment alone (fraction a, Table 2) nor the
spatially structured environment (fraction b, Table 2)
is the best predictor to explain NRI variation. The
space alone presented the higher fraction of explana-
tion for NRI variation (fraction c, Table 2), but the
unexplained fraction of variation was also high
(fraction d, Table 2).
Discussion
Despite some recent efforts (Vill
eger et al. 2010,
2012; Pease et al. 2012), functional diversity and
functional structure of tropical fish assemblages
remain poorly explored. For headwater streams, our
 Functional structure of rivers and streams
(a) Headwater streams (b) Rivers
0.70 0.8

0.65
0.7
0.60
0.6
0.55
MPD

0.50 0.5

0.45
0.4
0.40
R 2 adj = 0.23; p = 0.22 0.3 R 2 adj = 0.30; p = 0.16
0.35

0.30 0.2
0 5 10 15 20 25 30 35 0 5 10 15 20 25 30 35 40 45
S S
(c) (d) 7
6
6
5
R 2 adj = 0.20; p = 0.30 5 R 2 adj = –0.48; p = 0.02
4 4
3
NRI

3
2
2 1
1 0
–1
0
–2
–1 –3
0 5 10 15 20 25 30 35 0 5 10 15 20 25 30 35 40 45
S S
Fig. 3. Linear regression results between species richness and two functional indexes: MPD (a–b) and NRI (c–d). Linear regressions were
performed for headwater (a–c) and river (b–d) fish assemblages. R2 adj refers to adjusted R2 of the linear regression.

Table 1. Statistics of the multiple linear regression between the functional thermore, functional structure patterns showed that
structure index (NRI) and environmental variables (adjusted R² = 0.56, 34.5% of the headwater streams sampled had a sig-
P < 0000).
nificant functional clustering, but almost all of the
streams exhibited positive raw values for NRI indi-
Functional Variable entered in the model
structure index (sign of the effect) P N
cating a tendency of fish assemblages to clustering.
Taking into account that headwater streams habitats
NRI Channel depth ( ) 0.0002 49 are highly affected by local environmental conditions
Water velocity (+) 0.0000 49 (Ostrand & Wilde 2002; Grenouillet et al. 2004),
Dissolved oxygen ( ) 0.0005 49
Turbidity ( ) 0.0010 49 such as channel depth and water velocity (S
uarez
et al. 2007), it seems quite reasonable to think that
The sign of the effect indicates a positive (+) or negative ( ) effect of the environmental conditions drive the functional compo-
variable on the functional structure index.
sition patterns of local fish assemblages in this study.
If environmental conditions are leading to function-
Table 2. Results of variation partitioning on NRI values. ally clustered assemblages, then they are probably
acting as filters to fish species traits. In this case,
a b c d even assemblages with more species would be com-
posed of functionally similar species, and an increase
Fraction (%) 12.9 17.5 34.9 34.7
in species richness would not be accompanied by an
Fractions correspond to the variation explained by environment alone (a); increase in functional diversity or functional structure
environment spatially structured (b); space alone (c); and residuals (d). values. For rivers, functional trends were opposite to
Fractions are based on adjusted R squares (R2 adj) of each component. those observed in headwaters streams. Although only
27.3% of the rivers sampled displayed fish assem-
findings revealed that neither functional diversity nor blages with significant functional overdispersion,
functional structure of their fish assemblages is almost all of them presented negative raw values for
significantly correlated with species diversity. Fur- NRI suggesting a tendency to overdispersion. This

7
Carvalho & Tejerina-Garro
trend was partially explained by species diversity,
thus rivers with a higher number of species tend to
present a higher degree of functional overdispersion.
In general, habitat diversity and stability tend to
increase further downstream reaches (Meffe & Mink-
ley 1987; Jackson et al. 2001), and greater habitat
structural complexity can be associated with greater
morphological diversity (Willis et al. 2005). There-
fore, the functional overdispersion observed in rivers
may be a result of the increase in the number of spe-
cies with different functional traits due to habitat
structural complexity. Nevertheless, we suggest that
this proposal should be evaluated more carefully in
future investigations as the average species richness
found in this study for rivers was not much higher
than in headwaters. Moreover, species richness
explained only 48% of NRI trends suggesting that
functional structure in this type of habitat is probably
affected by other factors. If both habitat types
(streams and rivers) are likely to be affected by dis-
tinct ecological factors, the main question here is:
Which processes are most strongly affecting their
functional structure?
Several studies have pointed out a major role of
abiotic factors in shaping fish assemblages’ structure.
Peres-Neto (2004) showed that habitat features are
more relevant than species interactions to determine
species co-occurrence. Poff & Allan (1995) demon-
strated that trophic specialist fishes are more associated
with fish assemblages of stable watercourses, while
trophic generalists are more numerous at sites with
higher hydrological variability, whereas Hoeinghaus
et al. (2007) revealed that both habitat type and stabil-
ity have a powerful effect on fish assemblages and
their functional organisation. Our results pointed to
an important role of environmental variables on func-
tional structure variation in headwater streams and
rivers. More specifically, four of the eight variables
considered were strongly correlated with patterns in
functional structure: channel depth, dissolved oxygen,
turbidity and water velocity. Water velocity and oxy-
gen have been presented as possible selective filters
for species traits (Poff 1997). For headwater streams,
channel depth and water velocity are expected to
affect species co-occurrence because they restrict
events of colonisation and influence the persistence
of species in this kind of habitat (S
uarez et al. 2007).
Based on this background, we suggest that a potential
ecological process that might lead headwater stream
fish assemblages to functional clustering is environ-
mental filtering, and at least three environmental vari-
ables are good candidates to act as selective filters
for species functional traits: channel depth, water
velocity and dissolved oxygen. According to Poff
(1997), there are other environmental conditions that
may act in the selection of species traits such as: sub-
8
strate type and mobility, organic matter input, flood
intensity, extreme temperatures, etc. Future investiga-
tions should explore how the functional structure of
headwater streams fish assemblages is related to these
environmental parameters. For rivers, the association
between functional structure and environmental vari-
ables seems not to be clear as it is for headwaters.
The tendency for functional overdispersion observed
in rivers may be a consequence of the increase in
species traits diversity due to a higher habitat struc-
tural complexity (Willis et al. 2005). Given that
channel depth is usually considered as a good indica-
tor of habitat structural complexity (S
uarez et al.
2007), we suggest that this variable could also be
important for determining species co-occurrence in
rivers.
However, differences between headwater streams
and rivers related to environmental parameters are
often associated to an expressive altitudinal differen-
tial. In this study, sampled sites in both habitats have
similar levels of altitude, suggesting that the relation-
ship between the functional structure of fish assem-
blages and the environment can be even stronger
when the altitudinal gradient is more evident. In this
case, we could expect a higher level of functional
clustering in headwater streams.
Despite the significant role of the environment on
the functional structure of headwater streams and riv-
ers, it is worth noting that variation partitioning
results indicated a lower contribution of the environ-
mental component. Furthermore, both spatial and
spatially structured environment components showed
some contribution to functional structure variation.
Together, the spatial component and the spatially
structured environment are supposed to express the
influence of neutral dynamics on community struc-
ture (Gilbert & Lechowicz 2004; Diniz-Filho et al.
2012). A neutral process guided by species dispersal
limitations through the space is likely to occur
between headwater and river habitats. For example,
several species from rivers are not capable of reach-
ing headwaters, whereas headwaters are known to
support fish species that do not occur anywhere else
in the river system (Paller 1994; Meyer et al. 2007).
Moreover, fish assemblages sampled in this study are
located inside a region that is characterised by the
occurrence of many fish species with restricted spa-
tial range (Nogueira et al. 2010), in which dispersion
probably occurs at short distances. Finally, although
the focus of this study is on a local scale, the entire
set of our sampled sites is distributed between two
watersheds (Tocantins and Araguaia). Even if they
are capable of actively moving throughout different
habitats (Agostinho & Zalewski 1995), fish species
often have limited rates of dispersal between distinct
watersheds, which is imposed by the drainage area

itself or shifts in environmental conditions (Matthews
& Robison 1988; Jackson et al. 2001). Under these
circumstances, space also appears to play an impor-
tant role for the functional structure of headwater
streams and river fish assemblages. Limitations of
spatial species dispersion between headwaters and
rivers seem to be a potential cause for this. It is worth
to highlighting that the lower contribution of the
environmental component on variation partitioning
can be a consequence of the fact that variables are
spatially structured. Local variables as channel depth,
water velocity, turbidity and/or dissolved oxygen
may present different levels for headwater streams
and rivers (for example, rivers tend to have a deeper
channel than headwater streams).
It is necessary to consider the influence of two pos-
sible biases on the results. First, differences observed
between rivers and headwater streams may be influ-
enced by the different sampling methods used because
of the distinct remarkable features of the two habitats
sampled. This may facilitate plausible fish species
selectiveness and differences on total number of indi-
viduals sampled with potential consequences on spe-
cies and/or functional richness. The second bias is
associated with the use of field data for fulfilling
information about the functional data set, particularly
substrate preference and foraging location traits, that
may increase the association between functional indi-
ces and the environmental component. However, we
call attention that these are the best data available for
the fish assemblages sampled as inventories of the fish
fauna for the sampled region are incomplete (Tejeri-
na-Garro 2008) and far from being well documented
(Vari 1988; Revenga & Kura 2003), as observed for
freshwater ichthyofauna in other regions of the world
(L
ev^eque et al. 2005; Dudgeon et al. 2006).
Our findings suggest that there is a co-existence of
functionally similar species in fish assemblages of
headwater streams, whereas a co-existence of func-
tionally dissimilar species is more common in fish
assemblages of rivers. The environment seems to
play an important role in driving these functional pat-
terns and environmental filtering emerges as a poten-
tial ecological process in determining functional
clustering in headwater habitats. This selective force
would be guided by, at least, three main environmen-
tal variables: channel depth, water velocity and dis-
solved oxygen. For rivers, we argued that habitat
structural complexity might be the environmental
condition driving the co-existence of dissimilar spe-
cies as heterogeneous habitats may support species
with different traits. Nevertheless, our results revealed
that spatial components also play a key role in deter-
mining the functional trends in both habitat types.
We suggest that a neutral dynamic process linked to
species dispersal limitations between headwater
Functional structure of rivers and streams
streams and rivers may be the explanation, although
the spatial structure of environmental variables may
affect these patterns too. In this sense, the functional
structure patterns observed for headwater streams and
rivers are probably structured by both environment
and space. Finally, we found, excepting for a partial
contribution in the functional structure of river
assemblages, that species diversity is not related to
functional diversity and functional structure trends in
both headwater stream and river fish assemblages.
These findings are relevant for conservation of these
systems. If sites with high species diversity do not
harbour high functional diversity, the use of a conser-
vation strategy based on a single aspect of diversity
as a cure-all should be avoided.
This study opens the possibility for further and
challenging investigations, such as: (i) Are there
other environmental variables that may act as selec-
tive filters in headwater streams? (ii) Are environ-
mental variables selecting the same functional traits
in different fish assemblages, that is, are fish assem-
blages with functional clustering occupying the same
region of the functional traits space? (iii) Which func-
tional traits are more related to these selective envi-
ronmental variables? (iv) Which traits are more
related to the habitat structural complexity of rivers?
(v) How the altitudinal gradient may influence func-
tional patterns between headwater and river habitats?
Answering these questions will help us to understand
more completely how different processes are acting
on fish assemblages and how species traits are related
to them in both freshwater habitats.
Acknowledgements
We are grateful to all students, technicians and researchers
from Centro de Biologia Aqu
atica (CBA) that helped during
the fieldwork, especially Waldeir Francisco de Menezes. We
also thank Dr. Frabricio Barreto Teresa for helping us with
relevant suggestions in earlier versions of the manuscript; Dr.
F. Guillaume Blanchet who helped with the understanding of
the AEM framework and the construction of some R func-
tions; and Dr. Thiago Santos for several debates and ideas
about spatial analysis and R software. We thank to researchers
from Pontif
ıcia Universidade Cat
olica do Rio Grande do Sul
who assisted in species identification. We thank anonymous
reviewers for their contributions to improve the initial draft of
this study. To the National Council of Technological and Sci-
entific Development – CNPq for the financial support given
for the project (CNPq No. 471283/2006-1). RAC research is
supported with a scholarship by Coordenacß~ao de Aperfeicßoa-
mento de Pessoal de N
ıvel Superior – CAPES.
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12
Supporting Information
Additional Supporting Information may be found in
the online version of this article:
Table S1. Fish traits used to calculate mean pair-
wise distance (MPD) index of fish assemblages
located in headwater streams and rivers, Tocantins-A-
raguaia River Basin, Brazil.
Table S2. Description of the eight functional traits
and their respective categories used to calculate func-
tional diversity (MPD) and functional structure (NRI)
of headwater stream and river fish assemblages.
Table S3. Results found during NRI calculation
via null model approach for fish assemblages of
headwaters streams and rivers of the Tocantins-Ara-
guaia basin.