longitudinal variation of periphytic algal community structure in a tropical river

Longitudinal variation of periphytic algal community structurein a tropical river

Thais de Almeida Pereira • Sirlene Aparecida Felisberto •

Valeria de Oliveira Fernandes

Received: 2 August 2013 / Accepted: 21 October 2013

� Botanical Society of Sao Paulo 2013

Abstract The present study evaluated the influence of

abiotic factors on the periphytic algal community structure

under different environmental conditions. Six sampling sites

were established along the course of the Sao Mateus River:

two upstream of the city of Sao Mateus (E1, E2), two along

the city (E3, E4), and two downstream of the city (E5, E6).

Biotic and abiotic samplings were performed every week, in

September and October 2010, totaling four collections. The

periphyton was collected from roots of Eichhornia crassipes

(Mart.) Solms. removed by scraping with brushes and jets of

distilled water, fixed and preserved with formalin 4 %

(qualitative analyses) and with acetic lugol 5 % (quantitative

analysis). Higher richness of taxa and total density of peri-

phytic algal community were registered in the sampling sites

along and downstream of the city of Sao Mateus, with a

greater contribution of Bacillariophyceae (richness) and

Cyanophyceae (total density) in all sampling sites. The

periphytic algal density was influenced by nutrients (espe-

cially nitrogen) and turbidity, as evidenced by the CCA.

Thus, it is suggested that the input of allochthonous matter,

especially from human activities (intensive fish farming and

discharge of domestic and industrial wastewaters) change

the water quality (as evidenced by the PCA), as well as

communities of periphytic algae present.

Resumo O presente estudo avaliou a influencia dos fatores

abioticos sobre a estrutura da comunidade de algas perifıti-

cas submetidas a diferentes condicoes ambientais. Ao longo

do rio Sao Mateus, seis estacoes amostrais foram deter-

minadas: duas a montante da cidade de Sao Mateus (E1,

E2), duas ao longo da cidade (E3, E4) e duas a jusante da

cidade (E5, E6). As amostragens bioticas e abioticas foram

realizadas em intervalos semanais, em setembro e outubro/

2010, totalizando quatro coletas. O perifıton foi coletado de

raızes de Eichhornia crassipes (Mart.) Solms., removido por

raspagem, com pinceis e jatos de agua destilada, fixado e

preservado com solucao de formalina a 4 % (analise quali-

tativa) e com solucao de lugol acetico a 5 % (analise

quantitativa). Maior riqueza de taxons e densidade total da

comunidade de algas perifiticas foi registrada nas estacoes

amostrais ao longo e a jusante da cidade de Sao Mateus, com

maior contribuicao das Bacillariophyceae (riqueza) e Cya-

nophyceae (densidade total) em todas as estacoes amostrais.

A densidade total das algas perifiticas foi influenciada pelos

nutrientes (principalmente nitrogenio), assim como pela

turbidez, como constatado pela CCA. Assim, podemos su-

gerir que a entrada de material aloctone, proveniente prin-

cipalmente das atividades antropicas (piscicultura intensiva

e lancamento de efluentes domesticos e industriais) alteram

a qualidade da agua (como evidenciado na PCA), assim

como as comunidades de algas perifıticas presentes.

Keywords Anthropic impact � Bacillariophyceae �Cyanophyceae � Density

T. de Almeida Pereira (&)

Laboratorio de Taxonomia e Ecologia de Algas Continentais,

Departamento de Botanica, CCHN, Universidade Federal do

Espırito Santo, Av. Fernando Ferrari no. 514, Campo Goiabeiras,

Vitoria, ES CEP 29075-015, Brazil

e-mail: [email protected]

S. A. Felisberto

Programa de Pos-graduacao em Biodiversidade Vegetal,

Instituto de Ciencias Biologicas I, Universidade Federal de

Goias, Campus Samambaia, Caixa Postal: 131, Goiania, GO

CEP 74001-970, Brazil

V. de Oliveira Fernandes

PPGBV, Laboratorio de Taxonomia e Ecologia de Algas

Continentais, Departamento de Botanica, CCHN, Universidade

Federal do Espırito Santo, Av. Fernando Ferrari no. 514, Campo

Goiabeiras, Vitoria, ES CEP 29075-015, Brazil

123

Braz. J. Bot

DOI 10.1007/s40415-013-0034-1

Introduction

Aquatic ecosystems have been altered in different scales as

a result of natural processes and human activities. In this

sense, rivers (unidirectional ecosystems) are part of what

happens in the surrounding areas, considering the use, and

occupation of land (Silva et al. 2011). Thus, the limno-

logical characteristics of aquatic systems, particularly

biological communities, reflect information of anthropo-

genic disturbances (Calisto et al. 2001).

Human activities cause disturbances in communities of

aquatic systems which change abundance, species richness,

behavior, and physiological reactions (Agences de L0eau

1993), because the conditions of the aquatic environment

influencing the species (Leveque 1996). Since rivers are

subjected to several disturbances, ecological theories were

proposed to describe and understand their functioning,

aiming the better knowledge of the distribution of biotic

communities. Among them stands out the serial disconti-

nuity theory of Ward and Stanford (1983, 1995), which

postulates that a human interference, such as the con-

struction of reservoirs and dump of wastes, disrupts the

river gradient in relation to limnological conditions.

Especially in the littoral region of aquatic system, the

understanding of distribution patterns of periphytic algae is

essential; once they form the basis of the food chain (Battin

et al. 2003; Sandsten et al. 2005), work as reducers and

transformers of nutrients (Wetzel 1996), serves as habitat

and refuge for larval and juvenile, besides representing an

escape strategy for many predators (Fernandes and Esteves

2011) and are used to detect changes in the ecosystem, for

example, eutrophication (Mattila and Raisanen 1998),

since the periphytic algal have a short life cycle and form

of adhesion to the substrate, which prevents them from

adverse conditions (Castro et al. 2008).

By be very sensitive to changes in water quality and

hydrodynamics of the system, periphytic algae can be

qualitatively influenced by several abiotic variables: the

depth and suspended materials (Hardwick et al. 1992), the

current velocity (McIntire 1966; Acs and Kiss 1993), the

light (Scott and Scott 2000; Forsberg et al. 2001), and

phosphorus (Irvine and Jackson 2006; Iwaniec et al. 2006).

To Inove and Nunokawa (2005), light has a positive effect

on the development of periphyton, provided there are no

limiting nutrients; otherwise the increase of light does not

increase the biomass of periphyton.

In this way, physical and chemical variables play a very

strong environmental selectivity on the composition and

distribution of organisms, determining the species com-

position, and abundance (Matsumara-Tundisi and Tundisi

1997).

Considering that human interferences alter physical,

chemical, and biological natural conditions that lead to the

river discontinuity along stretches downstream and

upstream of cities (Silva et al. 2010), it is expected that

species richness and total density of the periphytic algal

community are higher in the downstream of the city of Sao

Mateus due to human activities and behaving in a discon-

tinuous manner along the stretches, as observed by Pereira

et al. (2013, subject) for abiotic data. In this way, the goal

of this study was to evaluate the influence of abiotic factors

on the structure of periphytic algal community.

Materials and methods

Study area

The Sao Mateus formed by the rivers Cotaxe (North Arm)

with about 244 km and Cricare (South Arm) with about

200 km (Fig. 1) is the major water supply for several cities

and has supplied water for several projects of irrigation,

and inevitably is also being used as receiver of domestic

and industrial waste of these and other locations (ANA

2009).

Samplings and abiotic and biotic analyses

Samplings were undertaken weekly in September and

October 2010, totaling four collections (September 08th,

15th and 22nd, and October 1st). Six sampling sites were

established along the course of Sao Mateus River, two

upstream of the city of Sao Mateus (E1, E2), two along the

city (E3, E4), and two downstream of the city, under the

influence of intensive fish farming and discharge of

domestic and industrial waste (E5, E6, respectively)

(Table 1). The periphyton was collected from roots of three

individuals (randomly taken) the floating aquatic macro-

phyte Eichhornia crassipes (Mart.) Solms in the littoral

region of each sampling site and removed from the sub-

strate with brushes and jets of distilled water. For quali-

tative analysis, samples were fixed with formalin 4 % and

for quantitative analysis, with acetic lugol 5 % (Bicudo and

Menezes 2006).

The climatic data (air temperature and rainfall) were

obtained from the weather station at the University Center

of North Espırito Santo. In the field, limnological variables

evaluated at each sampling station were conductivity

(lS cm-1) and dissolved oxygen (mg L-1) with YSI

multiparameter. Water samples were collected manually

with bottles in the subsurface of the water column a and

analyzed in the laboratory for analysis of turbidity (NTU)

with Alfakit V1.25 turbidimeter; pH (bench pH meter);

total suspended solids (mg L-1) according to APHA

(2005), total nitrogen (Valderrama 1981), nitrite (Gol-

terman et al. 1978), nitrate (Mackereth et al. 1978),

T. de Almeida Pereira et al.

123

ammonium ion, silicates (Carmouze 1994), orthophosphate

(Strickland and Parsons 1960), and total phosphorus

(Valderrama 1981), all in lg L-1.

Data analysis

The qualitative analysis of algae was performed from

samples mounted on temporary slides using optical micro-

scope Olympus CX 41 equipped with a camera lucida. Taxa

were sketched, photographed, measured, and identified

using the specific literature. The quantitative analysis, in

pseudoreplica (n = 2) was carried out using sedimentation

chambers (Utermohl 1958), using an inverted microscope in

random fields (Uehlinger 1964). Individuals were counted

until stabilizing the species accumulation curve and abun-

dant species with at least 100 individuals counted (Bicudo

1990). Each cell, colony or filament was considered a single

individual. Results were adapted from APHA (2005),

replacing the scraped area by the dry weight of the mac-

rophyte root, and expressed in ind.mg-1.

Fig. 1 Map of the Espırito Santo State, highlighting the Sao Mateus River basin and the location of the sampling sites (E1, E2, E3, E4, E5, E6)

(modified from satellite imagery, Google Earth)

Table 1 Characterization of

the sampling sites along the Sao

Mateus River

CESAN Espırito Santo’s station

company, SAAE Autonomous

water and sewage, APESAM

Fishermen’s Association of Sao

Mateus

Sampling

sites

Geographical

coordinates

Localization Features

E1 S 18�41.7030 Water uptake station CESAN Riparian Forest preserved

W 39�52.0840

E2 S 18� 42.2840 Before the bridge of the

BR101-North

Riparian Forest just preserved

W 39� 52.7280

E3 S 18� 42.8360 Station water intake—SAAE Urban core

W 39� 51.6420

E4 S 18� 42.6590 Historic site of the city Discharge of domestic

wastewater untreatedW 39� 51.2460

E5 S 18� 43.1120 Fish farming (net-cages)

APESAM

150 fish farming of tilapia

(Oreochromis sp.)W 39� 48.8530

E6 S 18� 43.2170 APESAM Discharge of domestic

and industrial wastewaterW 39� 48.8220

Periphytic algal in river

123

To check significant differences (p \ 0.05) between mean

values of biotic and abiotic variables of the sampling sites (i.e.

four replicate per site) it was applied the nonparametric

Kruskal–Wallis test, followed by the Dunn test to identify

which pair of sampling sites had these differences. These tests

were run in the software BioEstat (Ayres et al. 2007).

The principal component analysis (PCA) used to

examine the longitudinal variation relative to abiotic vari-

ables was performed with five variables (conductivity,

euphotic zone, silicate, nitrite, orthophosphate). For inter-

preting the results, we used the axes with eigenvalues

higher than of the Broken-Stick model (suggested by

Jackson 1993), as a consistent assessment to determine the

adequate number of components for interpretation.

The influence from the five abiotic variables (total

nitrogen, turbidity, total suspended solids, ammonium ion,

and silicate) on the distribution of periphytic algae (relative

abundance of 57 taxa) in the sampling sites of the Sao

Mateus River upstream up to downstream of the city was

investigated by a canonical correspondence analysis (CCA)

with the significance tested by a Monte Carlo test

(p \ 0.05) and 999 randomizations.

For PCA and CCA, the variables were log transformed,

and analyses were run with the software PC-ORD 5.15

(McCume and Mefford 2006).

Abundant and dominant species were determined

according to Lobo and Leighton (1986).

Results

The study period presented high temperatures (average of

22 �C) and low rainfall (average of 0.05 mm),

characterizing the period as dry and warm. The Sao Mateus

River had higher values of turbidity, total suspended solids,

conductivity, nitrite, ammonium ion, total nitrogen in the

sampling sites downstream of the city of Sao Mateus (E5

and E6) (Table 2).

Turbidity, conductivity, total phosphorus, nitrite, and

ammonium ion registered in the sites E5 and E6 were

significantly different (p \ 0.05) from the other sites. Total

suspended solids of the E6 were different from the other

sites; orthophosphate of the site E5 differed from the E2

and E3, while E6 significantly differed from the sites E1,

E2, E3, and E4. Regarding nitrogen compounds, the total

nitrogen of the sites E5 and E6 was significantly distinct of

the E1, E2, and E3; nitrate of the E1 differed from the E5.

Results of the PCA have explained 92.4 % of total data

variability on the first two axes (Table 3). On the axis 1

(73.3 % explanation), there was a distinction between

Table 2 Longitudinal variation of abiotic variables mean values (n = 4), followed by the standard deviation, registered in the sampling sites,

analyzed in September and October 2010

Variable E1 E2 E3 E4 E5 E6

pH 7.3 ± 0.1 7.3 ± 0.1 7.3 ± 0.2 7.2 ± 0.1 7.3 ± 0.1 7.3 ± 0.1

Turb (NTU) 14.5 ± 7.4 10.6 ± 4.0 9.5 ± 3.4 9.6 ± 4.2 36.3 ± 9.8 38.0 ± 9.4

EC (lS cm-1) 209.8 ± 6.3 213.7 ± 11.7 208.9 ± 5.9 214.0 ± 9.9 309.6 ± 75.6 275.0 ± 32.2

STS 3.2 ± 2.1 5.8 ± 4.0 2.7 ± 2.6 3.9 ± 1.8 19.5 ± 6.8 14.2 ± 11.9

Zeu 1.9 ± 0.5 2.1 ± 0.6 2.3 ± 0.5 1.9 ± 0.4 0.9 ± 0.5 0.6 ± 0.2

Transp 0.6 ± 0.2 0.7 ± 0.2 0.8 ± 0.2 0.6 ± 0.1 0.3 ± 0.2 0.2 ± 0.1

Si-SiO4 (mg L-1) 7740 ± 130 7615 ± 310 76180 ± 430 7242 ± 800 75770 ± 220 7202 ± 1150

TP (lg L-1) 33 ± 4 30 ± 10 35 ± 10 28 ± 9 67 ± 14 114 ± 47

P-ortho (lg L-1) 17 ± 4 11 ± 2 14 ± 3 15 ± 4 25 ± 40 67 ± 70

TN (lg L-1) 452 ± 20 519 ± 80 538 ± 70 607 ± 120 894 ± 110 866 ± 150

NO3- (lg L-1) 96 ± 40 108 ± 40 126 ± 50 151 ± 60 159 ± 30 127 ± 20

NO2- (lg L-1) 2 ± 2 3 ± 4 2 ± 1 1 ± 2 11 ± 3 13 ± 2

NH4? (lg L-1) 10 ± 4 14 ± 9 9 ± 5 16 ± 7 288 ± 42 329 ± 80

Turb turbidity, EC electrical conductivity, STS total suspended solids, Transp transparency, Zeu euphotic zone, Si-SiO4 silicate, TP total

phosphorus, P-orto orthophosphate, TN total nitrogen, NO3- nitrate, NO2

- nitrite, NH4? ammonium ion

Table 3 Correlation between abiotic variables and principal com-

ponents of the PCA

Results Axis 1 Axis 2

Eigenvalues 3.666 0.956

Broken-stick 2.283 1.283

Variables Eigenvalues

Electrical conductivity (C.E.) 20.9080 0.2128

Euphotic zone (Z.eu) 0.9924 -0.0671

Silicate (Si-SO4) 0.3121 0.9412

Orthophosphate (P-orto) -0.8818 -0.0884

Nitrite (NO2-) 20.9910 0.1128

Bold values indicate significant correlations


123

sampling sites, with E5 and E6 on the left of the axis, being

especially associated with conductivity, orthophosphate,

and nitrite. On the other hand, E2 and E3 have been pos-

itively related to euphotic zone (Fig. 2). Although with low

explanation (19.1 %), the axis 2 evidenced a clear dis-

tinction between sites upstream of the city (E1) and along

the city (E4), positively influenced by the higher values of

silica (Fig. 2).

Periphytic algal community in the Sao Mateus River

was comprised 149 taxa distributed into nine Classes.

Bacillariophyceae (diatoms) contributed most in number of

taxa (63), followed by Cyanophyceae (51), Zygnemaphy-

ceae (10), Chlorophyceae (8), Euglenophyceae and Oe-

dogoniophyceae (5), Ulothricophyceae (3), Chrysophyceae

(2), and Rhodophyceae (2).

Of the total of 149 taxa registered in the Sao Mateus

River, 23 were common to all sampling sites; 9 were

exclusive of the sites downstream of the city; 2 were

exclusive of the sites along the city; and 2 were exclusive

of those upstream of the city (Table 4).

In relation to the total density of periphytic algal com-

munity, higher mean values were observed in the site E4

(along the city of Sao Mateus) and E6 (downstream of the

city). The total density of the site E5 differed (p \ 0.05)

from the sites E1 and E4. The Class Cyanophyceae most

contributed for the total density in all sampling sites.

Bacillariophyceae was representative for total density, in

the sites E1, E4, E5, and E6 (Fig. 3), especially represented

by Gomphonema and Eunotia.

During the study period, Synechocystis aquatilis Sau-

vageau was the single dominant species in all sampling

sites, while Gomphonema turris Ehrenberg, Lyngbya sub-

tilis W. West, and Lyngbya orientalis (G. S. West)

Compere were abundant in E1; Limnothrix redekei (Van

Goor) Meffert was abundant in E3, Gomphonema neo-

nasutum Lange-Bertalot and Reichardt in E5, and Syn-

echococcus nidulans (Pringsheim) Komarek in E6.

The CCA has summarized 57.1 % of total abiotic data

variability (five variables, Table 5) and biotic data (57 taxa;

9). The eigenvalues associated with the first two axes were

0.30 and 0.23, corresponding to 32.4 and 24.7 % explana-

tion (respectively), with high significant relationship

(p \ 0.05) among variables used in the ordination (Fig. 4).

The correlations species-environment was 0.99 for both

axes. Abiotic variables correlated with the axes indicate an

environmental gradient, with sampling sites downstream of

the city (E5, E6), positively related with nutrients.

On the axis 1, the values of turbidity, total phosphorus,

orthophosphate, and ammonium ion have positively influ-

enced the site 6, and negatively the sites E2 and E3. On the

axis 2, the total nitrogen has negatively influenced the sites

E5 and E4 and inversely, E1. Several taxa of diatoms of the

Order Pennales, besides Encyonema silesiacum (Bleisch)

Mann, G. turris Ehrenberg, and G. turris var. coartata

(Frenguelli); filamentous cyanobacteria (L. subtilis W.

West) have had higher positive scores of the axes (related

to the site E1; Fig. 4), whereas L. redekei Author, Pseu-

danabaena minima (G. S. Anagnostidis) Anagnostidis;

Frustulia sp. 1; Frustulia sp. 2; Frustulia sp. 3; Pleurosira

laevis (Ehrenberg) Compere; Surirella robusta Ehrenberg;

Oscillatoria chalybea Mertens ex Gomont; Tetraedron

mininum (A. Braun) Hansgirg; Oscillatoria simplicissima

Fig. 2 PCA of abiotic variables for the sampling sites of the Sao Mateus River. C.E. electrical conductivity, Z.euf. euphotic zone, SiSO4 silicate,

NO2- nitrite, P-ortho orthophosphate


123

Gomont have had higher negative scores (related to sites

E2 and E3; Fig. 4). The axes have described a community

of periphytic algae with higher species richness mainly

distributed along and downstream of the city of Sao Mateus

(E4, E5 and E6; Fig. 4).

Discussion

The assessment of the longitudinal dynamics of physical

and chemical parameters can subsidize the better under-

standing of structure and functioning of river ecosystems

(Silva et al. 2010), and also ecological functions of diverse

groups of organisms (Power et al. 1988), because they are

adapted to the current environmental conditions and are

affected by any type of disturbance (Alba-Tercedor 1996),

since pollutants change physical and chemical character-

istics of water that affect continuity of system.

Human interferences in the sampling sites along and

downstream of the city of Sao Mateus possibly have influ-

enced the separation of the sites E5 and E6 from the others in

the longitudinal profile of the river, as evidenced in the PCA.

The input of allochthonous matter from intensive fish

farming (net cages) (near the E5) and from domestic and

industrial waste (near the E6) may have contributed with

increased turbidity, conductivity, total suspended solids, and

nutrients (total phosphorus, ammonium ion, nitrite, and total

nitrogen). The waste discharge acts as discontinuity factors

affecting the aquatic system, mainly at middle region and

downstream of the city (Silva et al. 2010). Thus, the

0

5000

10000

15000

20000

25000

30000

E1 E2 E3 E4 E5 E6

Den

sity

per

cla

ss(i

nd

.mg

- ¹)

Sampling sites

Cyanophyecae Bacillariophyceae Euglenophyceae Others

Fig. 3 Relative contribution of the Classes of periphytic algae to the

total density in the sampling sites, in September and October 2010

Table 4 List of taxa common and exclusive of the sites upstream

(E1, E2), along (E3, E4) and downstream of the city of Sao Mateus

(E5, E6)

Taxa E1 E2 E3 E4 E5 E6

Cyanophyceae

Aphanocapsa delicatissima W. et

G.S. West

X X X X X X

Chroococcus minor (Kutzing)

Nageli

X X X X X X

Cyanophyceae nonidentified 1 X X

Lyngbya aerogineo-caerulea

(Kutzing) Gomont

X X

Lyngbya cf. comperei (Meneghini)

Senna

X X

L. orientalis (G. S. West) Compere X X X X X X

Lyngbya perelegans Lemmermann X X

L. subtilis W. West X X X X X X

Oscillatoria bornetii (Zucal) Forti X X

Oscillatoria chalybea Mertens ex

Gomont

X X X X X X

Oscillatoria simplicissima Gomont X X X X X X

S. nidulans (Pringsheim) Komarek X X X X X X

S. aquatilis Sauvageau X X X X X X

Synechocystis minima Veronichin X X

Bacillariophyceae

Bacilaria paxilifera (Muller)

Marsson

X X X X X X

Calloneis sp.2 X X

Ciclotella meneghiniana Kutzing X X X X X X

Cocconeis fluviatilis Wallace X X X X X X

Eunotia flexuosa (Brebisson

in Kutzing) Berg

X X

Eunotia formica Ehrenberg X X X X X X

G. neonasutum Lange-Bertalot

and Reichardt

X X X X X X

Gomphonema lagenula Kutzing X X X X X X

G. turris Ehrenberg X X X X X X

G. turris var. coartata (Frenguelli) X X X X X X

Gyrosigma spencerii (Quick) Griff

and Henfrey

X X X X X X

P. laevis (Ehrenberg) Compere X X X X X X

Polymyxus coronalis Bailey X X X X X X

Surirella tenera Gregory X X

Synedra sp. 2 X X

Terpsinoe musica Ehrenberg X X X X X X

Ulnaria ulna (Nitzsch) Compere X X X X X X

Chrysophyceae

Mallomonas sp.2 X X

Zygnemaphyceae

Hyalotheca sp.1 X X

Rhodophyceae

Compsopogon sp.1 X X X X X X

Table 4 continued

Taxa E1 E2 E3 E4 E5 E6

Oedogoniophyceae

Oedogonium sp.4 X X X X X X

Ulothricophyceae

Ulothrix cf. tenerrima (Kutzing)

Kutzing

X X


123

Table 5 Statistical summary and correlation coefficients between periphytic associations and abiotic and biotic variables on the first two axes of

the CCA

Variaveis bioticas Codigo Coeficientes canonicos

Eixo 1 Eixo 2

E. silesiacum (Bleisch) D.G. Mann E. siles 1.308975 2.256995

Penalles 8 Penalles 1.308975 2.256995

Synechococcus elongatus (Nageli) Nageli S. elong 0.196820 -0.091505

S. aquatilis Sauvageau S. aquat -0.239118 0.063250

G. turris Ehrenberg G. turr 1.114696 0.416034

Aphanocapsa delicatissima W. et G.S West A. delic -0.089642 0.118318

G. turris var. coartata (Frenguelli) Frenguelli G. turri 1.082316 0.109207

Pennales 9 Pennales 1.308975 2.256995

Trachelomonas volvocinopsis Swirenko T. volvo 0.725317 0.056156

Polymyxus coronalis Bailey P. coron 0.715686 -0.368096

Cocconeis fluviatalis Wallace C. fluvi -0.239118 0.063250


Ciclotella meneghiniana Kutzing C. meneg -0.148078 -0.110510

Eunotia formica Ehrenberg E. formi -0.060112 0.005363

Terpsinoe musica Ehrenberg T. music -0.031348 0.171110

Eunotia pectinalis (Kutzing) Rabenhorst E. pecti 0.061218 0.562947

L. orientalis (G.S. Wet) Compere L. orient 0.634092 -0.235416

L. subtilis W. West L. subtil 1.308975 2.256995

Gomphonema lagenula Kutzing G. lagen -0.269763 -0.034186

S. nidulans (Pringsheim) Komarek S. nidul -0.316987 0.178239

Oscillatoria chalybea Mertens ex Gomont O. chaly -1.043759 1.082837

Oedogonium sp. 4 Oedogoni -0.520564 -0.520564

Frustulia sp. 1 Frustuli -1.745161 0.261434

P. minima (G. S. An) Anagnostidis P. minim -2.022074 0.627646

Oscillatoria simplicissima Gomont O. simpl -0.928167 -0.228203

Chroococcus minor (Kutzing) Nageli C. minor -0.067371 0.284365

Frustulia sp. 2 Frustuli -1.161065 -0.568942

Tetraedron minimum (A. Braun) Hansgirg T. mimin -0.936222 0.613398

Surirella robusta Ehrenberg S. robus -1.422843 -0.251705

Gyrosigma spencerii (Quek) Griff and Henfr. G. spenc 0.546818 0.029631

Eunotia veneris (Kutzing) De Toni E. vener 0.154694 -0.064102

Nitzschia palea (Kutzing) W. Smith N. palea -0.637508 -1.203416

Ulnaria ulna (Nitzsch) Compere U. ulna 0.117473 -0.049630

Choricystis chodatti Fott C. choda 0.015002 -0.141363

Achnanthes elata (Leuduger-Fortmorel) Gandhi A. elata -0.063452 -1.432799

Synedra sp. 1 Synedra -0.637508 -1.203416

Gomphonema contraturris Lange–Bertalot and Reichardt G. contr 0.049476 -0.693966

P. laevis (Ehrenberg) Compere P. laev -1.526125 -0.049957

Pinnularia sp. 1 Pinullar 0.968987 -0.964687

Calloneis sp. 2 Callonei 1.084661 -1.891567

Ulothrix tenerrina (Kutzing) Kutzing U. tener 1.007545 -1.273647

Mallomonas sp.2 Mallomon 0.533510 0.541136

Pennales 5 Pennales 0.356373 -0.426344


Pennales 3 Pennales 0.853313 -0.037808



123

continuity of the system is broken between the sites E5 and

E6 (an extremely impacted zone) in relation to physical and

chemical parameters of Sao Mateus River.

Thus, assessing the impacts upstream and downstream

the point of interest in the river is important because these

impacts affect the development of various organisms. In

this sense, the longitudinal variability pattern in rivers

influences the heterogeneity of organisms in the local

habitats, mainly algal periphytic, substrate dimensions, and

development of riparian vegetation (Komulaynen 2004b).

Excessive periphyton growth can occur in rivers and lakes

as a result of high water temperatures or excess nutrient

production from human development on the landscape,

agricultural operations, deforestation, and soil disturbance,

and therefore, can serve as an ecological indicator for these

disturbances (Bojsen and Jacobsen 2003; Cascallar et al.

2003; Giorgi and Malacalza 2002; Harding et al. 1999;

Siva and John 2002).

The highest number of Bacillariophyceae in the Sao Ma-

teus River, especially represented by the genera Gomphonema

and Eunotia (Pennales unicellular diatoms), was possibly due

to the greater amount of taxa abundant and dominant. This is a

group of algae well represented in most aquatic environments,

from temperate to tropical, including reservoirs (Cetto et al.

2004; Felisberto and Rodrigues 2005), rivers (Komulaynen

2008; Neves 2011; Felisberto and Rodrigues 2010, 2012), and

floodplain (Rodrigues and Bicudo 2001).

Diatoms are considered rapid and effective colonizers, and

a great part presents structure specialized to attach to the

substrate, such as long mucilaginous stalks as in Gompho-

nema, production of mucilaginous matrices as in Cymbella,

Encyonema, Frustulia, and Navicula, and colonies with star-

shaped, branches, attached by the basis, as in Eunotia and

Fragilaria (Cetto et al. 2004). The highest richness of this

group in the sampling sites of the Sao Mateus River is prob-

ably related to these structures that provide competitive

advantage to diatoms compared with other algal groups. Still,

diatoms are regarded as fast and efficient colonizers; the

substrates being covered within a period of a day to several

weeks (Felisberto and Rodrigues 2012). Moreover, high

concentration of silica in all sampling sites of Sao Mateus

River can be benefited to diatoms, since the silica is a com-

pound of fundamental importance for the frustules of diatoms

(Esteves et al. 2011). This fact can be evidenced, mainly for E.

silesiacum (Bleisch) Mann, G. turris Ehrenberg, and G. turris

var. coartata (Frenguelli) that were related to site E1 (CCA)

which was associated by the higher values of silica (PCA).

The high density of Cyanophyceae in the periphytic

algal community of the Sao Mateus River is probably

accounted for species of Synechocystis (dominant), the

filamentous genera, especially Lyngbya and Limnothrix,

and high concentration of nutrients. Cyanophyceae often

play an important role in attached communities in running

waters (Acs et al. 2003), being primarily represented by

ruderal species (r-strategist), with optimal development for

long periods (Reynolds 1984). Still these prokaryotes are

associated with high temperatures, thermal stability of the

environment, and availability of nitrogenous compounds

(Fonseca and Rodrigues 2007).

Environments with high concentration of nitrogen favor

the development of filamentous algae (Lampert and Sommer

2007), since filaments are excellent adaptive forms that grow

rapidly in length, and can remain with constant area/volume

ratio (Margalef 1983). This fact can be corroborated by the

expressive richness of Cyanophyceae in the Sao Mateus

River, mainly represented by the genera Oscillatoria and

Lyngbya which were common to all sampling sites.

Clearly describe what, how, and when limnological

variables control the growth and development of periphytic

algal community is very complex. This is because several

limnological factors are often restricted and measured in free

water, not on the substrates, where the water composition is

Table 5 continued

Variaveis bioticas Codigo Coeficientes canonicos

Eixo 1 Eixo 2


L. redekei (Van Goor) Meffert L. redek -2.208178 0.700006

Pinnularia sp. 2 Pinnular -1.68462 0.065532

Geitlerinema sp. 1 Geitleri 0.061819 0.355145

Koliella longiseta (Vischer) Hindak K. longi 0.223576 -1.547491

Chlorella vulgaris Beijerink C. vulga 0.223576 -1.547491

Frustulia sp. 3 Frustuli -1.835970 0.555286

Calloneis sp. 1 Callonei 1.084661 -1.891567

Bacillaria paxilifera (O.F.Muller) T.Marsson B. paxil 1.084661 -1.891567

Eunotia flexuosa (Brebisson in Kutzing) A. Berg E. flexu 1.084661 -1.891567

Synechocystis minima Veronichin S. minim 1.084661 -1.891567


123

Fig. 4 Ordination by the CCA

of abiotic A and abiotic

B variables, analyzed for the six

sampling sites along the Sao

Mateus River. NT total nitrogen,

NH4? ammonium ion, Turb

turbidity, P-ortho

orthophosphate, PT total

phosphorus


123

influenced by the community. Thus, in the Sao Mateus

River, the input of allochthonous matter (intensive fish

farming and discharge of domestic and industrial waste) into

the sites along and downstream of the city consisted in

essential factors that promoted remarkable effects on the

values of richness and density of periphytic algae, influenced

by nutrients (nitrogen and phosphorus, in general) and tur-

bidity (as evidenced by the CCA), leading to discontinuity in

the system. Therefore, the initial hypothesis was corrobo-

rated, i.e., the species richness and total density of periphytic

algal community have had higher values in stretches

downstream of the city of Sao Mateus.

Acknowledgments The authors thank to the Fishermen Association

of the Juara Lagoon for logistic support and help, to the Laboratory of

Taxonomy and Ecology of Freshwater Algae (LATEAC) for labora-

tory analysis and to the Laboratory of Environmental Sciences

(UENF)—Ecology Laboratory, for helping in analyses of nutrients,

and to CAPES (Coordination of Improvement of Higher Education

Personnel) and to the Graduate Program in Tropical Biodiversity, for

the scholarship to the first author.

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