International Research Journal of Plant Science (ISSN: 2141-5447) Vol. 4(3) pp. 64-75, March 2013
Available online http://www.interesjournals.org/IRJPS
Copyright © 2013 International Research Journals
Full Length Research Paper
Comparison of the structure of the periphytic
community in distinct substrates from a neotropical
floodplain
1
Stefania Biolo and 2Liliana Rodrigues
1
Universidade Estadual Paulista "Julio de Mesquita Filho", Biosciences Institute, Av 24-A, 1515, Bela Vista, 13506-900,
Rio Claro, São Paulo, Brazil
2
Universidade Estadual de Maringá, Núcleo de Pesquisas em Limnologia Ictiologia e Aquicultura, Av. Colombo, 5790,
Bloco G-90, 87020-900 Maringá, Paraná, Brasil
Abstract
Periphyton collected from distinct macrophytes in a lake permanently connected to the Paraná River
were submitted for analysis of the periphytic algae community structure, quarterly in the years 2008
and 2009. Limnological data were concomitantly measured. Flood pulses, hydrometric levels of the
Paraná river and hydrological periods were irregular in 2008. It was found 406 taxa of periphytic algae,
with greater richness corresponded mainly to the classes Bacillariophyceae and Zygnemaphyceae. The
mean values of richness were not significantly different among substrates (p=0.297; F=1.342), but were
for algal density (p=0.037; F=4.390) and diversity on Eichhornia azurea (Sw.) Kunth; Pontederiaceae),
probably due to its architecture and morphology being more suitable to the development of periphytic
algae, mainly diatoms. Oxycarium cubense, due to its fragile architecture and delicate morphology,
favoring mainly metaphytic algae as Zygnemaphyceae. In June and September 2008, Bacillariophyceae
was prevalent (predominantly represented by Achnanthidium minutissimum (Kütz.) Czarn.
(Bacillariophyceae), which could represent a greater tolerance of these microalgae during unfavorable
periods. Mean values of diversity were significantly different after November 2008, with higher average
values of the hydrometric levels and temperatures. It concluded that, in an extreme variable
environment, such as the floodplain, although significant differences have been found, both the
environmental conditions and the type of substrate were essential for structuring the periphytic
community.
Keywords: Periphyton, attached algae, natural substrates, aquatic macrophytes, open lake, Brazil.
INTRODUCTION
Aquatic macrophytes are key components of inland
waters because they affect nutrient cycling and contribute
to enhancing habitat complexity (Dibble et al., 2006),
which increases freshwater biodiversity (Bonecker et al.,
1998; Pelicice et al., 2008). These attributes highlight the
positive effects that several types of wetlands (including
river-floodplain systems), which are highly colonized by
macrophytes, have on biodiversity conservation (Padial
et al., 2009). The periphytic community can be influenced
by availability and diversity of substrates in the
*Corresponding
Author
E-mail:sbiolo@gmail.com
environment, especially macrophytes (Pizarro, 1999;
Algarte, et al., 2009; Ferreira et al., 2011). Different
species of macrophytes act as substrates with particular
physiological and morph structural characteristics, which
in turn can or cannot influence periphyton community
associated (Cattaneo et al., 1995, 1998; Laugaste and
Reunanen, 2005; Kulesza et al., 2008).
In the extremely heterogeneous ecosystems of
floodplains, their environments are limnological and
biologically characterized in a variant way, due to the
action of flood pulses or hydrosedimentological pulses
(Thomaz et al., 2007). Structure and dynamics of the
periphytic community are under the influence of the
amplitude, frequency, and intensity of these pulses.
Biolo and Rodrigues 65
The inherent resistance to the study of the periphyton
community in macrophytes, or epiphyton (Stevenson,
1996), can be attributed in part to the high spatial
heterogeneity of these communities and consequent
methodological problems of sampling (Townsend and
Gell, 2005). It is a fact that the spatial heterogeneity of
the periphyton community present in macrophytes
interferes with the study of this community in order to
predict the factors affecting the structure and dynamics of
the periphyton precisely (Lalonde and Downing, 1991;
Vadeboncoeur et al., 2006). The substrate itself
constituted by macrophytes may make studies difficult,
since seasonal changes in plant growth and hosts affect
the surface area for colonization by the periphyton
community (Wetzel, 1983; Goldsborough and Hickman
1991; Pizarro 1999).
However, as highlighted by Messyasz and KuczynskaKippen (2006), there are quantitatively insufficient studies
about the structure and dynamics of epiphyton in different
macrophytes. In the Paraná River floodplain, only three
studies contemplate this approach, including the latter
part of this research (Tesolín and Tell, 1996; Mormul et
al., 2010, Biolo and Rodrigues, submitted). Given the
paucity of works, their importance extends from the
record of diversity of the periphyton substrates and their
complementation analysis of biodiversity in the riversystem floodplain (Nabout et al., 2007).
Comprising first steps to provide information for
understanding of the periphyton between different
substrates on the Paraná River floodplain, the following
macrophytes were sampled: Eichhornia azurea (Sw.)
Kunth (Pontederiaceae), Nymphaea amazonum Martius
and Zuccarini (Nymphaeaceae) and Oxycaryum cubense
(Poepp. and Kunth) K. Lye) (Cyperaceae). This work is
part of the dissertation of the first author, wich the present
study aimed to investigate the species richness,
abundance and diversity of the periphytic algae in these
different substrates, contributing to knowledge of the
macrophyte-periphyton complex. The hypothesis that
underlies this study is that the mean values of density,
species richness and diversity of periphytic algae, in the
same environment, differ between different natural
substrates, at any given time. Thus, we assess the
significance of presence of different substrates which in
turn is reflected in the diversity of the periphytic
community, under the influence of flood pulse
macrofactor.
MATERIALS AND METHODS
Natural substrates for collecting periphyton consisted of
macrophyte petioles in the adult stage of the following
species (and ecological groups), according to Irgang et
al. (1984): E. azurea (emerging) and N. amazonum
(floating fixed), and the stem of Oxycaryum cubense
(epiphyte). In O. cubense, the leaf sheath involved in the
region of stem was also sampled. Selection of substrates
was done as following: their presence in a same bank,
presence of multi-species under similar environmental
conditions, and in all sampling periods. In addition to
presenting similar morphostructural characteristics, we
attempted to standardize sampling methodologies (which
could be equally applied to all substrates according to
their morphology). We also aimed to supply the lack of
studies of the periphytic community encompassing the
last two substrates cited in the Paraná River floodplain.
Substrates collected consisted of replicates (n=2). For
removal of the periphytic community of substrates, a steel
blade coated on an aluminum sheet with the aid of jets of
distilled water was used. Material designated to
qualitative analysis was fixed in Transeau solution, while
for quantitative analyses, acetic lugol solution 5% was
used.
Abiotic variables sampling
Abiotic variables were simultaneously measured during
the collection of biological material and corresponded to:
water temperature and dissolved oxygen (oximeter YSI
model 55 laptop brand), pH (portable pH meter model
Digimed DM2), electrical conductivity (Conductivity
Digimed laptop model DM2), alkalinity (Carmouze, 1994),
transparency of the water column (Secchi disk), turbidity
(Turbidimeter portable model Lamotte), total solids,
organic and inorganic fractions (Wetzel and Likens,
1991), total nitrogen and nitrate (Bergamin et al., 1978;
Giné et al., 1980), ammonia nitrogen (Mackereth et al.,
1978), and total phosphorus (Mackereth et al., 1978) and
phosphate (Mackereth et al., 1978). For analysis of the
fraction of dissolved nutrients and suspended solids
determination, we filtered samples using Whatman GF-C
52 filters (Golterman et al., 1978). Data of the
hydrometric level of Paraná River were obtained by the
measurement of the rule relating to the São José Port,
Paraná. Abiotic data were ceded by the Laboratory of
Limnology, at NUPELIA (“Núcleo de Pesquisas em
Limnologia Ictiologia e Aquicultura”) and other details
about the sampling methodology are shown in Roberto et
al. (2009).
Study area and periphyton sampling
Periphyton analysis
The Pau Véio Lake is an open lake with a permanent
connection to the Paraná River, Brazil (22o44'S 53o15'W). Sampling of the periphytic community was
performed quarterly between June 2008 and March 2009.
Qualitative analysis of the periphytic algae proceeded
through preparation of permanent slides and their
analysis under light microscopy (Bicudo and Menezes,
66 Int. Res. J. Plant Sci.
Table 1. Abiotic data from the Pau Véio lake, at the Upper Paraná River floodplain, in the period of study
June 2008 to March 2009 (Biolo & Rodrigues, submitted).
Temperature (ºC)
Dissolved oxigen (mg.L-1)
pH
-1
Condutivity (µS.cm )
-1
Alcalinity (µEq L )
Mean hydrometric level (m)
Transparency (Secchi) (m)
Turbidity (NTU)
Total solid matherial (µg.L-1)
-1
Total nitrogen (µg.L )
-1
Nitrate (µg.L )
Ammoniacal nitrogen (NH4+)
Total phosphorus (µg.L-1)
-1
Orthophosphate (µg.L )
JUN
19.4
6.15
6.83
56.7
468
2.95
3.1
3.33
2.1
227.5
135.8
4.9
13.2
4.9
2006). Taxa found were identified based on classical and
regional literature. Classification systems adopted
comprehending Round (1965; 1971) recommended by
Bicudo and Menezes (2006). For quantitative analysis,
the algal count was performed according to the Utermöhl
method (1958), using an inverted microscope and
chambers of sedimentation. The count used delimited
horizontal and vertical transects, in random fields, with
the quantification of 100 individuals of the species most
common and rarefaction curves of species, as proposed
by Bicudo (1990). Very concentrated samples were
diluted to facilitate visualization and counting of
individuals. Unicellular organisms, colonies, filaments,
and cenobium were considered as individuals.
Data analysis of the periphytic community
Structural attributes of the periphytic algae community
were species richness (number of taxa), density (number
2
of individuals per cm ) according to the equation of Ros
(1979), adapted to the area of the substrate; specific
diversity of the community through the Shannon Diversity
-1
Index (H ') and expressed in bits.ind , and evenness (E).
The diversity index was calculated using the program PCOrd 4.0.
Detrended Correspondence Analysis or Correspondence
Analysis with removal of the arc effect (DCA) was used
for the dominant species frequency of occurrence and
abundance above 50% (Lobo and Leighton, 1986). The
DCA were performed using the program PC-Ord 4.0.
Between axes of the DCA, significant differences were
tested using the Mann-Whitney test (non-parametric, p
<0.05), within the program Statistica 7.1 (Statsoft Inc.,
2005), and data were Log2 transformed when necessary.
To test for significant differences in density, richness, and
SEP
20.9
4.31
6.55
59.3
457.5
2.55
2.2
0.6
368.1
97.9
2.6
12.1
3.7
NOV
27.1
2.59
6.62
59.9
387.2
2.39
2
2.28
0.75
495.2
45.8
19.3
18.6
13.8
MAR
28.5
5.22
6.91
58.8
410.4
3.16
2.25
3.63
1.88
1000.9
120.7
7.26
20.6
5.5
diversity, two-way ANOVA was used to determine the
effect of factors and the interaction of factors on attributes
(normality with the Shapiro-Wilk test, normal distribution
and homoscedasticity, the Levene's test, p> 0.05). When
no significant interactions between factors were found,
we applied the Tukey test a posteriori. The two-way
ANOVA and all graphics were performed in Statistica 7.1
(Statsoft Inc., 2005).
RESULTS
Abiotic data
Data relating to abiotic variables in the Pau Véio Lake,
during the study period, are summarized in Table 1 and
the values of hydrometric levels in Figure 1.
The year 2008 was characterized by an irregularity in
hydrological periods of high water (November to May)
and low water (June to October), with the prevalence of
low values throughout the year. In 2009, the period of
high water was characteristic, from the elevated levels in
January, with peaks above the level of overflow in
February 2009 (between 3.53 and 4.65 m). More
discussions were presented in Roberto et al. (2009) and
Biolo and Rodrigues (submitted). Jointly, the similarity of
the specific composition of the periphytic algal community
in the three substrates in the Pau Véio Lake were
detailed in Biolo and Rodrigues (submitted).
Periphytic
substrates
algal
community
structure
among
The mean values of total species richness showed no
significant difference in relation to different substrates,
Biolo and Rodrigues 67
Figure 1. Daily hydrometric levels from the Paraná River in the
period of study June 2008 to March 2009, in the morning and
afternoon. Arrows indicate the days of sampling (06/28/2008,
07/29/2008, 11/28/2008, and 03/13/2009), and the dashed line marks
the overflow level (3.5 m).
Table 2. Influence of factors (period; substrate; period x substrate) in the mean
richness of periphytic algae verified by two-way ANOVA. Values with an
asterisk indicate a significant difference (p <0.05).
Factors
Period
Substrate
Period x Substrate
D.F. (effect; error)
3; 12
2; 12
6; 12
however the opposite was observed for the sampling
periods (p=0.0003; F=13.459) (Table 2, Figure 2). When
assessing the effect of both substrate and period in the
richness of the periphytic algae, it showed the average
interaction (p=0.0197; F=3.997) (Table 2, Figure 3) and
means were significantly different.
The total density of periphyton was delineated
confirming the change in density of the class
Bacillariophyceae, for both substrates and periods
(Figure 4). A large peak in the abundance of
Bacillariophyceae was recorded in E. azurea in
September 2008 (1042 103ind.cm-2). In all substrates and
periods, Achnanthidium minutissimum (Kütz.) Czarn.
(Bacillariophyceae) was the taxon responsible for the
highest values of density of the class Bacillariophyceae.
This peak in the mean density of Bacillariophyceae was
responsible for the differentiation of the periphytic
community in accordance with the type of substrate
(p=0.037; F=4.390) (Table 3, Figure 5).
This fact characterized the substrate of E. azurea as
presenting the most abundant algal density (except in
November 2008, which was N. amazonum) and the
F
13.459
1.342
3.997
P
0.00038*
0.2978
0.0197*
period of September 2008, while the lowest values were
in O. cubense and the period of March 2009 (Figure 6
and 7). Thus, significant differences between the mean
values of perifiphytic algal density in the substrates were
especially related between E. azurea and O. cubense (p
= 0.029) (Table 3; Figure 5).
Cyanobacteria comprised the second most abundant
group (278.5 103ind.cm-2) among all substrates and
periods, in general. Main classes following in abundance
corresponded to Zygnemaphyceae (90.8 103ind.cm-2)
3
-2
and Chlorophyceae (78.8 10 ind.cm ).
An oscillation was observed in the values of diversity
and evenness between the substrates and the three
sampling periods (Figures 8 to 10). E. azurea presented
the greatest variations among the sampling periods, while
in N. amazonum and O. cubense a tendency to increase
the values was observed. Significant differences were
due to mean diversity values of the periphyton community
present in E. azurea in September 2008 (p=0.041;
H=20.3) of other substrates. The mean values of
evenness did not differ significantly between the periods
and substrata.
68 Int. Res. J. Plant Sci.
Figure 2. Effect of the sampling period in total
richness of the periphytic algae in the Pau Véio lake.
Value in rectangle indicate significant difference by
Fischer's test (p <0.05). Mean values with bars
indicating the confidence interval (± 0.95).
Figure 3. Effect of the period versus the substrate in
total richness of the periphytic algae in the Pau Véio
lake. Value in rectangle indicate significant difference by
Fischer's test (p <0.05). Mean values with bars
indicating the confidence interval (± 0.95).
Figure 4. Mean density and standard deviation of
all classes, class Bacillariophyceae and the taxon
Achnanthidium minutissimum (Bacillariophyceae),
in the three substrates (EA = E. azurea, NA = N.
amazonum, and OC = O. cubense) and sampling
periods in the Pau Véio lake.
Biolo and Rodrigues 69
Table 3. Influence of factors (period; substrate; substrate x period) in the
density of periphytic algae (Log2) verified by two-way ANOVA. Values with
asterisk indicate a significant difference (p <0.05).
Factors
Period
Substrate
Period x Substrate
D.F. (effect; error)
3; 12
2; 12
6; 12
F
1.851
4.390
1.134
Figure 5. Effect of substrates in total density
(log2) of periphytic algae in the Pau Véio lake.
The values in the rectangle indicate significant
differences by Fischer's test (p <0.05). Mean values
with bars indicating the confidence interval (± 0.95).
Figure 6. Mean values of total density of the
periphytic algae for each period including all
substrates. S.D. = standard deviation.
Figure 7. Mean values of total density of the
periphytic algae for each substrate in the Pau
Véio lake. S.D. = standard deviation.
p
0.192
0.037*
0.399
70 Int. Res. J. Plant Sci.
(8)
(9)
(10)
Figures 8-10. Evenness (E), Shannon-Wiener
Diversity (H '), and Simpson diversity (D) of the
periphytic algae community in the three substrates
sampled (E. azurea, figure 8; N. amazonum, figure 9;
and O. cubense, figure 10) in the Pau Véio lake during
June 2008 to March 2009. Means are bars indicating
the standard deviation. Note the different scales.
Ordination analysis of the periphytic algal community
Detrended Correspondence Analysis or Correspondence
Analysis with removal of the arc effect (DCA) was applied
to the density of abundant and dominant taxa in the
different substrates and periods (Figures 11-12). Axes 1
and 2 of the DCA (eigenvalues 0.4457 and 0.1162,
respectively) for the species were significantly different
according to the Mann-Whitney test (p=0.036; Z=2.094).
We observed the ordination of samples by different
periods but not substrates (Figures 11-12).
Periphytic algal communities present in June and
Biolo and Rodrigues 71
(11)
(12)
Figures 11-12. Distribution of samples in relation to the abundant and dominant taxa and that frequently occurring
above 50%, in the Pau Véio lake (EA = E. azurea, NA = N. amazonum, and OC = O. cubense), figure 11; 1.
Achnanthidium minutissimum (Kütz.) Czarn.; 2. Encyonema mesianum (Chol.) Mann; 3. E. silesiacum (Bleis.) Man.; 4.
Eunotia faba (Ehr.) Grun.; 5. E. intermedia (Krass. ex Hust.) Nörp. & Lange-Bert.; 6. E. maior (W.Sm.) Rab.; 7. E.
neomundana Metz. & Lange-Bert.; 8. E. pectinalis (Dillw.) Rab.; 9. Fragilaria capucina Desm.; 10. F. tenera (W. Smith)
Lange-Bert.; 11. Gomphonema brasiliense Grun.; 12. G. clevei Fricke; 13. G. gracile Ehr.; 14. G. parvulum (Kütz.)
Kütz.; 15. G. truncatum Ehr.; 16. Navicula cf. trivialis Lange-Bert.; 17. Nitzschia amphibia Grun.; 18. N. linearis Grun.;
19. N. palea (Kütz.) Smith; 20. Ulnaria ulna (Nitzsch.) Comp. (Bacillariophyceae); 21. Chlorophyceae cocóide não
identificada 2 (Chlorophyceae); 22. Salpingoeca sp. (Chrysophyceae); 23. Cryptomonas cf. tenuis Pasch.
(Cryptophyceae); 24. Aphanocapsa parasitica (Kütz.) Komárek & Anagn.; 25. Chroococcus minor (Kütz.) Nägeli; 26.
Leibleinia epiphytica (Hieronymus) Anagn. & Komárek; 27. Leptolyngbya foveolarum (Gom.) Anagn. & Komárek; 28.
L. perelegans (Lemmerm.) Anagn. & Komárek; 29. L. angustissima (W. & G. S. West) Anagn. & Komárek; 30.
Phormidium molle Gom.; 31. Pseudanabaena frigida (Fritsch) Anagn. (Cyanobacteria); 32. Oedogonium sp.; 33.
Oedogonium sp. 4 (Oedogoniophyceae); 34. Characiopsis aquinolaris Skuja; 35. C. elegans Ettl (Xanthophyceae); 36.
Cosmarium subadoxum (Zygnemaphyceae), figure 12.
September 2008 were more similar; whereas in
November 2008 and March 2009 were more similar to
each other and significantly different compared to
previous months (Axis 1). Dominant periphytic algae in
March 2009 were different from other months according
to Axis 2 (Figure 11). Microalgae with greater dominance
were represented mainly by Bacillariophyceae and
Cyanobacteria (Figure 12). Aphanocapsa parasitica
(Kütz.) Komárek and Anagn. (Cyanobacteria) and
Cryptomonas tenuis Pasch. (Cryptophyceae). were
positively correlated to Axis 1 and Achnanthidium
minutissimum (Bacillariophyceae) negatively to this axis.
Eunotia intermedia (Krass.) Nörp. and Lange-Bert.
(Bacillariophyceae). and Phormidium molle Gomonth
(Cyanobacteria) were positively correlated with Axis 2,
whereas
Eunotia
silesiacum
(Bleis.)
Mann
(Bacillariophyceae) and Fragilaria tenera (W. Smith)
Lange-Bert. (Bacillariophyceae) negatively to this axis
DISCUSSION
Abiotic data
The Pau Véio Lake was characterized by its low
concentrations of nutrients (mainly phosphorus fractions)
and high transparency of the water column in this study.
This fact was previously reported for the Paraná River
and its adjacent environments by Roberto et al. (2009).
According to the first component of DCA, community
positioned relating in the first sampling periods (June and
September 2008) was different from those of the second
period (November 2008 and March 2009). The first two
months were characterized by low temperatures and
hydrometric levels, greater transparency and dissolved
oxygen concentration, and lower concentration of
nutrients (except for nitrate). Availability of nutrients, light,
and temperature, among other factors, are fundamental
to structuring and functioning of aquatic communities
(Thomaz and Bini, 1998).
Moreover, occurrence of flood pulses on upper
ParanáRiver floodplain in 2008 was irregular, with values
of the hydrometric levels reported in 2008 not consistent
with the typical segregation of hydrological periods.
Therefore, this year was primarily characterized by daily
fluctuations in the hydrometric levels and other
limnological variables, as previously presented by
Roberto et al. (2009) and Biolo and Rodrigues
(submitted).
72 Int. Res. J. Plant Sci.
Periphytic algal community structure
These conditions represented a greater degree of stress
on the periphytic community in 2008, which was probably
responsible for the lower value of total richness of
microalgae in June this year. In addition, this fact allowed
dominance of microalgae more tolerant to stresses such
as Bacillariophyceae, Cyanobacteria, and coccoid forms
(mainly represented by Chlorophyceae). The class
Bacillariophyceae was responsible for the higher
densities, unlike the richness that was the largest fraction
represented by Zygnemaphyceae (Biolo and Rodrigues,
submitted). Green microalgae and cyanobacteria have
also been well documented; these classes can come to
dominate
periphytic
community
under
certain
environmental conditions (Stevenson, 1996; Rodrigues
and Bicudo, 2004; Rodrigues et al., 2008; McCormick,
2011), corroborated in this work.
In connected environments, the highest density of
periphytic algae occurs in the upper Paraná River
floodplain, mainly due to density values of diatoms
(Rodrigues and Bicudo, 2001). In this study, the pattern
of total density of periphyton was defined by the density
of this group, especially resulting from a single species,
A. minutissimum. This taxon has been reported to be
dominant in other studies around the world (Comtè et al.,
2005; Laugaste and Reunanen, 2005; Zheng and
Stevenson, 2006; Karosienė and Kasperovičienė, 2008).
Effect of Homogenization on the periphytic algal
community
In the subsequent months (November 2008 and March
2009), the limnological conditions showed an
improvement, especially with rising temperatures,
hydrometric levels, and nutrient concentrations.
According to the second component of the DCA and
results of the Mann-Whitney tests, the year 2009 was
different from the year 2008. In fact, in 2009 the
occurrence of pulses of higher intensity may have
promoted changes in limnological factors and in the
periphytic community.
Greater influence of the Paraná River, through the
effect of homogenization (Thomaz et al., 2007), may
have promoted greater entry and establishment of algal
propagules in the environment (Rodrigues and Bicudo,
2001). Still, the pulses act as a major disturbance to the
increase in algal diversity by promoting the reduction of
dominant classes and the development of others
(Rodrigues and Bicudo, 2001; Algarte et al., 2009).
Thereby, higher values of richness and density for
other algal classes have been reported in the present
study during these periods, especially Zygnemaphyceae.
Increasing of richness of desmids as well as the
presence of microalgae such as Cryptophyceae (typically
of lentic habitats in this floodplain) and Rhodophyceae
(typical of high water and lotic environments) can be the
result of greater influence of the Paraná River on the lake
(Rodrigues and Bicudo, 2001). It is also attempted for
resuspension of desmids from sediment by convection
currents in periods of greatest incidence of pulses. These
currents introduce to surface algal with major biovolume
under the process of sedimentation or from epipelic
habits, present in deeper layers of the water column,
increasing algal diversity (Facca, 2002). These abiotic
factors may have influenced the periphyton community,
by conferring variability to the periphytic community in
different substrates this year.
Substrate influencing the periphytic algal community
With respect to substrate as a factor that structures the
periphyton community (Wetzel, 1983; Moschini-Carlos,
1999), the importance of this relationship is a subject
frequently discussed in the ecology of periphyton (Jones
et al., 2000, Pals et al., 2006). Particular species of
macrophytes differ markedly in their architecture,
morphology, and density of the macrophyte bank and
these differences are important factors that influence their
associated biota, especially periphyton (Messyasz and
Kuczynska-Kippen, 2006; Vis et al., 2006). Among the
main characteristics of substrate that can influence the
periphyton community present, the architecture and plant
morphology assume an important position, being
defended by some authors (Eminson and Moss, 1980;
Blindow, 1987; Lalonde and Downing, 1991; Zimba and
Hopson, 1997; Cattaneo et al., 1998; Jones et al., 2000;
Albay and Akcaalan, 2003; Gosselain et al., 2005;
Vadeboncoeur et al., 2006; Messyasz and KuczynskaKippen, 2006; Zhang et al., 2012).
Segregation of the periphytic community in
accordance with the type of substrate - especially for
architecture and microtopography of macrophyte - could
be observed in this study when analyzing the density,
richness, and diversity of periphytic algae. This is
because of the significant interaction effect result
between period and type of substrate according to the
Anova results on the richness of periphytic algae, and
total density means differed specifically between E.
azurea and O. cubense. Mean values of diversity of algal
community present in E. azurea, in September 2008,
were significantly divergent from the others.
With respect to E. azurea, such morphostructural
characteristics that may be acting to promote variability to
periphyton, include: i) the petiole covered by a rigid,
smooth, and resilient epidermal cuticle that could allow a
better adherence and retention of the periphytic
components and the formation of the periphytic matrix;
according to the results of this study, influencing the
dominance of diatoms, which were benefited by petioles
with more rigid structure (Laugaste and Reunanen,
2005). These microalgae secrete or present structure to
Biolo and Rodrigues 73
fixation cells and mucilaginous stalks that attach directly
to the substrate by secretion of mucilage (Rodrigues and
Bicudo, 2001), ii) orientation of plant branches under the
surface of water column (Cook, 1990) (stoliniferous
species) and formation of large banks that can minimize
the disturbance effect of watercourses on both
communities, which may be a selection factor for
periphytic algae that grow there; and iii) position of
macrophytes in which stems are floating and monitor the
level of the water column (Cook, 1990), preventing the
community from being exposed to desiccation or shading
of the plant structure itself.
Although N. amazonum presents stem morphology
apparently similar to the plant of E. azurea (flat and
cylindrical), different substrates have distinct spatial
distributions in the same environment and differ in their
physical and temporal stability (Lowe and Pan, 1996;
Vadeboncoeur et al., 2006). N. amazonum in a
comparative way in the present study may consist of a
substrate less resistant than E. azurea. This is probably
due to its thinner and epidermal cuticle and its delicate
vertical direction in the water column, which may bring
the petiole to shading by floating the leaf of this species
(Cook, 1990). At the same time, this makes the petiole
susceptible to a greater intensity of disturbance such as
water currents. Lowe and Pan (1996) demonstrated that
the littoral zone of shallow areas suffers constant
disturbances caused by the action of currents, resulting in
dominance of microalgae capable of adhering firmly to
the substrates. These characteristics may have promoted
a lower abundance of periphytic algae in N. amazonum
compared to E. azurea.
However, the substrate of N. amazonum further
provides a periphyton qualitatively more similar to the E.
azurea that O. cubense (Biolo and Rodrigues, submitted).
More relevant in N. amazonum, in a peculiar way, was
the class Oedogoniophyceae, which is important because
individuals promote an increase in the mosaic structure of
the periphytic microhabitat. It is because it increases the
spatial heterogeneity by allowing the epiphytism by other
microalgae, as the representatives of Chrysophyceae
and Xanthophyceae, and loosely attached microalgae
(Zygnemaphyceae) (Murakami et al., 2009).
In relation to the structure of O. cubense, this
substrate exhibited the lowest mean density among all
algal classes and substrates; however, this substrate had
higher
values
of
richness,
especially
of
Zygnemaphyceae. Plants of O. cubense may be
epiphytic on other macrophytes, such as E. azurea (V.J.
Pott and A. Pott, 2000). This habit may confer, to this
substrate, instability in front of disturbances of the water
column, such as hydrometric level variation and the
presence of currents. Thus, the permanence and
development of algal taxa in the periphyton community
may have been interfered with. Morphology of the wavy
stem and presence of a leaf sheath may also be
a selective factor to algal adhesion. However, plant
morphology (presence of leaf sheath covering the stem)
may have provided a different microhabitat. This allowed
development of mainly loosely attached microalgae, such
as Zygnemaphyceae, which were well represented in this
substrate.
Diversity of the periphytic algae
Diversity of periphytic algae in the Pau Véio Lake was
high, especially in November 2008 and March 2009.
Agostinho et al. (2000) emphasized the great biological
diversity found in the Paraná River floodplain, sustained
in this ecosystem mainly by changes in the hydrometric
levels. Increased diversity as well as richness in the
periods during this study was probably due to increased
temperature (Murakami et al., 2009), in the average
values of hydrometric levels and in concentrations of
nutrients, mainly phosphorus and nitrogen (Rodrigues
and Bicudo, 2001). Due to the direct communication of
the sampling environment to the Paraná River, there still
may be contribution of propagules carried to the
environment and increasing the pool of species
(Rodrigues et al., 2004). High levels of eutrophication
may be a factor in the decreased variety of microalgae
(Zheng and Stevenson, 2006); however, the study
environment may be characterized as mesotrophic
(OECD, 1982), which may have contributed to the high
values of diversity. In general, diversity was low in June
and September 2008 on all substrates, as a result of
dominance of Bacillariophyceae and high richness and
low abundance of classes of rare taxa. In studies with
large numbers of rare taxa with low abundances, it can
be attributed to the structural heterogeneity of the
periphytic community for various reasons, such as
stochastic factors associated with the colonization
process, exclusive competition for best-adapted taxa,
insufficient sampling, and substrate specificity (Townsend
and Gell, 2005).
While the diversity values were lower in E. azurea,
especially in September 2008, when this substrate was
more differentiated from other communities, other
substrates could include higher values of diversity, in
case N. amazonum and O. cubense in the same period.
In other months, species diversity in O. cubense reached
values the same as or higher than in E. azurea and N.
amazonum, due mainly to the higher contribution of
Zygnemaphyceae and other rarer classes for the
community on this substrate. Complex architecture of
macrophytes, which favors higher values of periphyton
biomass according to previous studies by Cattaneo and
Kalff (1980), Lalonde and Downing (1991), Gross et al.
(2003), can promote the highest average diversity of
periphytic algae, as in the present study. This fact
strongly indicates importance of diversity of substrates
in the environment for the diversity of periphytic algae,
as previously verified by Rodrigues et al. (2004) and
74 Int. Res. J. Plant Sci.
Murakami et al. (2009).
CONCLUSION
It is suggested that substantial differences in periphyton
present in different macrophytes are due to the
combination of biotic and abiotic factors prevailing at any
given time in the environment in which they occur (Pip
and Robinson, 1981, Kiss et al., 2003; Messyasz and
Kuczynska-Kippen, 2006). The hypothesis of the present
study was partially accepted, except for the species
richness, which differed between study periods (but not
among substrates). In an extreme variable environment,
such as the floodplain in the present study, both the
environmental conditions and the type of substrate were
predominant for structuring the periphytic algal
community, which is the opposite to what some authors
suggest, i.e., that the substrate is of secondary relevance
for structuring periphyton in front of abiotic conditions
(Eminson and Moss, 1980; Lalonde and Downing, 1991;
Albay and Akcaalan, 2003; Kiss et al., 2003; Pals et al.,
2006; Vadeboncoeur, 2006; Díaz-Olarte et al., 2007).
Furthermore, we conclude that the macrophyte E.
azurea - preferably and standardly used in ecological
analyzes of the periphytic community on the Paraná
River floodplain (Schwarzbold, 1990) – consist in a
suitable substrate for analysis of its attached community,
because
of
its
stable
morphostructure
and
methodologically satisfactory sampling of the periphyton.
ACKNOWLEDGEMENTS
This research project was inserted in the PELD –
“Pesquisas Ecológicas de Longa Duração, CNPq, A
Planície Alagável do Alto Rio Paraná- Site 6”. Authors
thank CAPES for granting the master scholarship to S.
Biolo and CNPq for the productivity fellowships to L.
Rodrigues. Authors also thank to scientific professionals
from NUPÉLIA (Núcleo de Pesquisas em Limnologia
Ictiologia e Aquicultura) for assistance in the
development of the present work, especially Vanessa
Majewski Algarte and Eveline A. Ferreira.
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