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Acta Scientiarum http://periodicos.uem.br/ojs/acta
ISSN on-line: 1807-863X
Doi: 10.4025/actascibiolsci.v41i1.45872
ECOLOGY
Colonization of benthic invertebrates on artificial and natural
substrate in a Neotropical lotic environment in Southern
Brazil
Nilce Svarcz Jungles de Camargo1, Atsler Luana Lehun2*, Jonathan Rosa2 and Ana Carolina de Deus
Bueno-Krawczyk1
Departamento de Ciências Biológicas, Universidade Estadual do Paraná, União da Vitória, Paraná, Brazil. 2 Programa de Pós-Graduação em Ecologia de
Ambientes Aquáticos Continentais, Núcleo de Pesquisas em Limnologia, Ictiologia, Universidade Estadual de Maringá, Av. Colombo, 5790, 87020-900.
Maringá, Paraná, Brazil. * Author for correspondence. E-mail: atslerluana@gmail.com
1
ABSTRACT. The objective of this research was to validate the colonization process on natural and
artificial substrates by benthic invertebrates in a tropical stream in South Brazil. The samples were
performed in July and August-2012, and 32 samplers were used, being 16 natural and 16 artificial
substrates. In each sample, two replicas were taken for each substrate at the 2th, 4th, 7th, 14th, 21th 28th, 35th
and 42th days of colonization. The organisms were identified to the lowest possible taxonomic level. In
both substrates 3,070 benthic invertebrates were detected, of which 1,753 individuals were collected on
the natural substrate, and 1,317 on the artificial substrate. From the identified taxa 8.5% were not
dominant (Anacroneuria, Orthocladiinae, Tupiara, Smicridea, Baetodes, Tupiperla, Macrogynoplax,
Gripopteryx, Cylloepus, Macrelmis, Microcylloepus, Hetaerina, Argia, Coryphaeschna, Atopsyche, Pomacea,
Corydalus, Leptohyphes and Eccoptura), and 31.5% were dominant (Tanypodinae, Chironominae, and
Paragripopteryx). The genus Simulium was very common, dominant and abundant, representing 65% of the
collected individuals. No significant difference was found in the abundance and species composition
between artificial and natural substrates. On the natural substrate, the higher colonization index was at
the 35th day with 459 individuals, and the lowest was at the 14th day, with 87. On the artificial substrate the
highest index was at the 42th day with 337 individuals, and the lowest was at the 4th day, with 85. Both
natural and artificial substrates are efficient in characterizing the benthic community. In the evaluation of
the ecological succession, it was not possible to observe a pattern that described the process, since the
composition was nearly constant throughout the study period.
Keywords: Community structure; Diversity; Tropical stream; Limnology; Simulium.
Received on February 25, 2019.
Accepted on June 24, 2019.
Introduction
Studies about diversity of the invertebrates in lotic environments integrate this ecological system as a
whole, especially considering understanding the interaction among different taxonomic groups in aquatic
communities. Benthic community has an important role in nutrients cycling and energy flux at the
ecosystems since they participate on the organic matter fragmentation, decomposition and allow the
ecological succession process (McCafferty, 1983; Bouchard Jr., 2004; Strixino & Trivinho-Strixino, 2006;
Lisboa, Silva, & Petrucio, 2011; Bagatini, Delariva, & Higuti, 2012).
Based on the occupied habitat, aquatic invertebrates can be differentiated as planktonic that are
associated with the water column or the surface film, and benthic, which are associated to the bottom and
adjacent substrates (Weber, 1973).
The composition and spatial distribution of benthic aquatic invertebrates’ fauna are related to several
environmental factors, highlighting the water flow and the type of substrate. The water flow may act on the
substrate nature, interfering in the structure of invertebrate communities (Whitton, 1975).
The succession process in environment begins when the organisms colonize a new substrate, in response
to the physical priorities (Braccia, Eggert, & King, 2014). This succession dynamics in a peculiar area is
initially recognized by the presence of less specialized taxa, also called pioneer organisms. They can change
Acta Scientiarum. Biological Sciences, v. 41, e45872, 2019
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Camargo et al.
the site characteristics and determine the colonization by other individuals which extinguish their
precursors (Carvalho & Uieda, 2004). Throughout the time this ecological succession process with the
replacement of a community by another, involves not only a change in the composition of species, but also
changes in biomass and environmental characteristics (Brower & Zar, 1984; Carvalho & Uieda, 2004).
The knowledge about the colonization process, richness and community structure of benthic
invertebrates can be obtained by the use of substrates (Rosenberg & Resh, 1982; Ribeiro & Uieda, 2005).
Several studies use natural and artificial substrates to characterize benthic fauna (Casey & Kendall, 1996;
Santos, Bruno & Santos, 2016). Inorganic substrates have determinants in colonization as the size and
surface, and the organic substrate has the feeding function, fixation and shelter (Rezende, 2007).
The artificial substrates are good to demonstrate primary succession process in the community and its
structure (Carvalho & Uieda, 2004). The use of these samplers is efficient because it facilitates
standardization of the sampling area and the time of the colonization. They are also important to evaluate
the dynamics of aquatic invertebrates in relation to the environmental conditions they are exposed, such as
the flow water of the stream and fluctuations of water level (Rodríguez, Becares, Soto, & Pacho, 1998).
Taking into consideration the importance of the substrates, we aim to evaluate the effect of natural and
artificial substrate on the richness, composition and abundance of the benthic invertebrate community in a
neotropical stream.
Material and methods
Study area
This study was conducted in a longitudinal section of Papuã River, a tributary of the Iguaçu River (26ºS
07’04.1” and 51ºW 09’58.5”) at União da Vitória, Paraná, South of Brazil (Figure 1). Papuã River is 4 meters
wide and about 58 cm deep. According to the river classification of Tundisi and Tundisi (2008) it is a small
stream of 2nd to 5th order. The vegetation cover is present on both sides, composed mainly of Araucaria moist
forest vegetation. It has an extensive rocky area, with rapids, shallow wells and sand near the banks, with
little foliage and gravel, which permit to test succession process in an aquatic ecosystem with natural
conditions.
All the replicas were taken in July and August 2012, during the low rainy period. The region climate is Cbf
humid subtropical, according to the Köeppen classification. The average monthly rainfall was about 140 mm.
Figure 1. Location of the study area in the Papuã River, Paraná, Brazil.
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Colonization of benthic invertebrates on substrates
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Sampling
As the composition of the substrate of the Papuã River is predominantly rocks, sand and few leaves and
gravel, we used artificial and natural substrates. Each artificial substrate consisted of a rectangular (8.0 × 6.0
× 2.5 cm) concrete block, with a total area of 210 cm 2, composed of cement (40%), fine sand (40%) and rocks
(20%). Each natural substrate consisted of a set of nine river rocks, each about 2.8 cm in diameter, washed
and dried on a wire mesh (1 cm mesh), with the total surface adapted to (1.5 × 1.2 cm) substrate (Carvalho &
Uieda, 2004; Delonzek & Krawczyk, 2016).
In the study area 32 sample units were used, being 16 natural and 16 artificial, with a distance of 1.5
meter between the substrates. Two replicates of each type of substrate (artificial and natural) were removed
from the stream at the 2th, 4th, 7th, 14th, 21th 28th, 35th and 42th days of colonization (Carvalho & Uieda, 2004).
The substrates removed from the water were individualized and stored in plastic containers, identified and
fixed in 10% formalin. In the laboratory, the sample units were washed and brushed in plastic trays. The
material obtained from the washing was filtered using a 0.25 mm mesh sieve, sorted under illuminated tray
and preserved in 70% ethanol.
The benthic organisms were identified to the lowest possible taxonomic level using stereoscopic
microscope and specialized identification keys (Trivinho-Strixino & Strixino, 1995; Merrit & Cummins,
1996; Mugnai, Nessimian, & Baptista, 2010; Trivinho-Strixino, 2011). The identified organisms were
deposited in the collection of the Zoology Laboratory of the Universidade Estadual do Paraná.
Data analysis
We analyzed data regarding the frequency of the individuals, abundance and dominance. We calculated
the dominance on the dominance limit (LD), and with the resulting value compared to the frequency of each
taxon. Frequencies smaller than the dominance limit (LD=4) is considered non dominant, while higher
frequencies are said dominant (Silveira Neto, Nakano, Barbin, & Villa Nova, 1972). The relative frequency
was calculated from each group present in relation to the total of individuals, considering that the taxa
relative frequency is the result of the division of the number of individuals of a taxon by the total number of
collected specimens (Dajoz, 1973).
The abundance of taxa was based on the calculation of the confidence interval on the number of the
samples (Vieira, 1980). The following categories were assigned for the taxa: rare (<624 individuals);
dispersed (≥ 864 individuals); common (≥ 891 individuals) and plentiful (≥1,131 individuals). The T test (p <
0.05) was applied to verify differences in abundance when compared to natural and artificial substrates. For
this analysis, in each sampling, the number of individuals in each replicate of the two types of substrates
was pooled separately, totalizing 8 samples of the natural substrate, and 8 samples of the artificial
substrate.
Rarefaction curves were performed according to the number of individuals, in order to compare the
species richness amongst the natural and artificial substrate at comparable levels of density (Gotelli &
Colwell, 2001), using the program biodiversity professional version 2 (2018).
A Principal Coordinates Analysis (PCoA) was performed to evaluate the (dis)similarity of species
composition between the substrates (natural and artificial). For the analysis, the axes were retained,
according to the criteria of broken-stick method. The samples scores of the axes 1 and 2 were submitted to
the Student’s t test to assess the significance differences of species compositions between natural and
artificial substrates. PCoA was carried out in R 3.4 software (R Development Core Team, 2016) using the
vegan (Oksanen et al., 2019) and permute (Simpson, 2019) packages. Analyze of variance (Student’s t test)
were performed in Statistica 7.1 (Statsoft Inc., 2005).
Results
A total of 3,070 individuals were recorded on both substrates (natural and artificial). Both substrates
used showed a significant number of individuals, 1,753 on natural substrate and 1,317 individuals on
artificial substrate (Table 1). In the analysis of abundance throughout the colonization process, there was no
significant difference between the two substrates (T test; p = 0.20), reinforcing the similarity between
substrates (Figure 2).
Acta Scientiarum. Biological Sciences, v. 41, e45872, 2019
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Camargo et al.
Figure 2. Mean values of the abundance found in the natural and artificial substrates during the colonization period. Bars represent
standard error and same letters in columns indicate no statistical significance.
Table 1. Benthic invertebrates collected in artificial and natural substrates, over 42 days of colonization in Papuã River, União da
Vitória - Paraná. (TF: individual frequency)
Taxa
Diptera
Simuliidae
Chironomidae
Plecoptera
Gripopterygidae
Perlidae
Ephemeroptera
Baetidae
Tricorythidae
Coleoptera
Elmidae
Odonata
Calopterygidae
Coenagrionidae
Aeshnidae
Trichoptera
Hydrobiosidae
Hydropsychidae
Mollusca
Ampularidae
Megaloptera
Corydalidae
Subfamily/genus
Natural
substrate
TF (%)
Artificial
substrate
TF (%)
Simulium
Chironominae
Tanypodinae
Orthocladiinae
1139
135
171
18
65
7.7
9.8
1
696
156
167
24
53
11.8
12.6
1.8
Paragripopteryx
Tupiperla
Gripopteryx
Anacroneuria
Macrogynoplax
Eccoptura
181
4
2
55
1
9
10.3
0.22
0.15
3.13
0.05
0.5
163
10
3
50
6
5
12.4
0.75
0.22
3.8
0.45
0.4
Baetodes
Tupiara
Leptohyphes
9
7
0
0.5
0.4
0
6
13
1
0.45
1
0.07
Macrelmis
Cylloepus
Microcylloepus
1
1
6
0.05
0.05
0.35
0
2
5
0
0.15
0.4
Hetaerina
Argia
Coryphaeschna
1
0
0
0.05
0
0
1
1
1
0.07
0.07
0.07
Atopsyche
Smicridea
1
12
0.05
0.7
0
5
0
0.4
Pomacea
0
0
1
0.07
Corydalus
0
0
1
0.07
The rarefaction curves demonstrated that benthic invertebrate richness reached an asymptote in two
type of substrates. The natural and artificial substrates showed similar numbers of individuals and taxa, but
the highest richness was recorded in the artificial substrate (Figure 3).
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Colonization of benthic invertebrates on substrates
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Figure 3. Rarefaction curves of benthic invertebrates in the sampling in substrate artificial and natural.
In both substrates the order Diptera was dominant. On natural substrate the species Simulium
represented 65% and on artificial substrate 53%, Tanypodinae on natural substrate with 9.8% of
representation and on artificial with 12.6%, Chironominae on natural 7.7% and on artificial 11.8%, followed
by Paragripopteryx (Plecoptera) represented 10.3% on natural substrate and on artificial substrate 12.4%, the
other taxa presented a number below than 4% in each substrate.
The genera Pomacea, Corydalus, Argia, Coryphaeschna and Leptohyphes were colonized only in artificial
substrate, while Macrelmis and Atopsyche colonized the natural substrate. Comparing the artificial and
natural substrates, we noticed that both presented a similar number of taxa over a period of 42 days of
colonization, although the values in numbers of individuals were higher in natural substrate.
The colonization pattern on substrates were similar on both substrates, this suggests that diversity
samplings in Papuã River can be done using these gears. The area showed 22 taxonomic groups less frequent
and one very frequent (Table 2).
Table 2. Abundance and dominance of the taxa of benthic invertebrates in Papuã River, União da Vitória - Paraná.
Subfamily/Genus
Simulium
Chironominae
Tanypodinae
Orthocladiinae
Paragripopteryx
Tupiperla
Gripopteryx
Anacroneuria
Macrogynoplax
Eccoptura
Baetodes
Tupiara
Leptohyphes
Macrelmis
Cylloepus
Microcylloepus
Hetaerina
Argia
Coryphaeschna
Atopsyche
Smicridea
Pomacea
Corydalus
Total
1835
291
338
42
344
14
5
105
7
14
15
20
1
1
3
11
2
1
1
1
17
1
1
Abundance
Plentiful
Rare
Rare
Rare
Rare
Rare
Rare
Rare
Rare
Rare
Rare
Rare
Rare
Rare
Rare
Rare
Rare
Rare
Rare
Rare
Rare
Rare
Rare
Dominance
Dominant
Dominant
Dominant
Non dominant
Dominant
Non dominant
Non dominant
Non dominant
Non dominant
Non dominant
Non dominant
Non dominant
Non dominant
Non dominant
Non dominant
Non dominant
Non dominant
Non dominant
Non dominant
Non dominant
Non dominant
Non dominant
Non dominant
Frequency
Very frequent
Less frequent
Less frequent
Less frequent
Less frequent
Less frequent
Less frequent
Less frequent
Less frequent
Less frequent
Less frequent
Less frequent
Less frequent
Less frequent
Less frequent
Less frequent
Less frequent
Less frequent
Less frequent
Less frequent
Less frequent
Less frequent
Less frequent
Acta Scientiarum. Biological Sciences, v. 41, e45872, 2019
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Camargo et al.
The genera Simulium and Paragripopteryx and the ones from the subfamily Chironominae and
Tanypodinae united had a frequency of 91.5% of all taxa sampled, consequently becoming the most
recurrent within the taxa studied. While Orthocladiinae showed 1% and the other genera was less frequent.
The genus Simulium represented 60% of all collected individuals, presenting the highest frequency of
individuals in the studied area, this genus is followed by: Paragripopteryx and Tanypodinae with 11%, and
also having a significant representation Chironominae with 9.5%. These are in the families Simuliidae,
Gripopterygidae and Chironomidae with the highest number of individuals.
The genus Anacroneuria had a frequency of 3.4% and Orthocladiinae 1.4%. The genera with frequency
below 1% was: Tupiara, Smicridea, Baetodes, Tupiperla, Macrogynoplax, Gripopteryx, Cylloepus, Macrelmis,
Microcylloepus, Hetaerina, Argia, Coryphaeschna, Atopsyche, Pomacea, Corydalus, Leptohyphes and the species
Eccopturaxanthenes.
In this study, among the samples 8.5% less frequent, non-dominant and rare, are represented by
nineteen taxa: Anacroneuria, Orthocladiinae, Tupiara, Smicridea, Baetodes, Tupiperla, Macrogynoplax,
Gripopteryx, Cylloepus, Macrelmis, Microcylloepus, Hetaerina, Argia, Coryphaeschna, Atopsyche, Pomacea,
Corydalus, Leptohyphes and Eccopturaxanthenes. Represented by two subfamilies: Tanypodinae and
Chironominae and by one genus: Paragripopteryx 31.5% less frequent, dominant and rare.
Higher colonization indexes of natural substrate were: at the 2nd day with 353 individuals, at 28th day
with 376, at 35th day with 459, and at the 42nd day with 335, the lowest index was at the 14th day of
colonization (n=87). On artificial substrate the higher colonization indexes were: at the 2 nd day with 167
individuals, at 7th day with 119, at 14th day with 155, at 28th with 139, at 35th with 228, and at the 42nd with
337, the lowest index was at the 4th day of colonization with 85 individuals (Figure 4).
Figure 4. Total number of individuals in each type of substrate per day of colonization in Papuã River, União da Vitória - Paraná.
The results of PCoA did not show significant differences in the dissimilarity of species composition of
the benthic invertebrates between the natural and artificial substrate (p > 0.05) (Figure 5). Thus, the
composition was similar during the colonization process on both substrates.
Discussion
In our study there were few differences between abundances and total numbers of taxa on the natural
and artificial substrates. Although there are no significant differences between both substrate types, some
taxa were exclusive to the artificial substrate, such as Mollusca and Megaloptera. Probably this type of
substrate provides a higher habitat heterogeneity, due to the interstitial spaces formed during the
preparation of the substrate, favoring the colonization of exclusive taxa. Carvalho and Uieda (2004) also
found no differences between both types of substrate (artificial and natural), but recorded exclusive taxa in
the artificial substrate. According to Anjos and Takeda (2005), the higher structural complexity of the
substrate favours the increase of species richness due to greater availability of resources and habitats.
A reduction in number of individuals was observed after the 4 th day of colonization. Abiotic and biotic
environmental conditions can reduce the abundance of aquatic invertebrates (Thomazi, Kiifer, Ferreira
Acta Scientiarum. Biological Sciences, v. 41, e45872, 2019
Colonization of benthic invertebrates on substrates
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Junior, & Sá, 2008), for example, predation by fish is a factor controlling the abundance of invertebrates in
streams (Lovell, Fletcher, Cooper, & McArthur, 2017). However, in this study, no change was observed in
the abiotic conditions of the environment during the colonization process, but the biotic variables were not
measured in the field and may be a possible factor responsible for the reduction of organisms.
Figure 5. Composition’s Dissimilarity of the benthic invertebrate’s community in natural and artificial substrates.
Among the several groups found, Diptera is the most widely distributed and frequently the most
abundant group in freshwater environments (Armitage, Cranston, & Pinder, 1995). In this study, it was the
most representative group, being present throughout the sampling period and presenting no difference by
substrate preference.
There was a prevalence of three families with a more significant number of individuals registered:
Simuliidae and Chironomidae (Diptera), Gripopterygidae (Plecoptera) which can also be corroborated in
studies such as Carvalho and Uieda (2004), Ribeiro and Uieda (2005), Pereira et al. (2010), where abiotic
factors influence the ecological structuring of aquatic biotopes, determining the occurrence and distribution
of organisms and their structuring.
Lisboa et al. (2011) and Rocha, Medeiros and Andrade (2012) described that Chironomidae was
distributed in subfamilies Chironominae, Tanypodinae and Orthocladiinae, and these taxa were the most
constant and diverse in community, especially because these families have distinct morpho-behavioral
characteristics (Silva, Pauleto, Talamoni, & Ruiz, 2009; Trivinho-Strixino & Strixino, 1995). Furthermore,
there are reports indicating that Chironomidae tends to increase during dry season (Aburaya & Callil, 2007),
which happened in this study, probably as a result of the preservation of the riparian forest around the river
and, consequently, great food availability.
Chironomidae are the most representative of aquatic insects as a result of the range of habitat
occupancy; the use of various resources, which confers adaptive strategies to colonize different types of
micro-habitats by different genera of the family (Trivinho-Strixino & Sonada, 2006). This wide range of
occurrence in terms of Chironomidae can be explained by their diversified eating habits (Armitage et al.,
1995). In general, the Chironomidae family does not require any special substrate for its development
(Entrekin, Wallace, & Eggert, 2007).
The genus Simulium showed to be well adapted to the environment, which allows it to bear several
abiotic factors. According to Ribeiro and Uieda (2005) rainfall was the factor that influenced the most the
structuring of benthic community. As in the rainy season, the rocky substrate and the Simuliidae, are
subjected to the direct action of the current, these taxa probably migrate and seek shelter on the vegetable
substrate. Most species are found on the underside of rocks, branches, or leaves living in fast-moving waters
(Statzner, 1981).
The abundance of aquatic invertebrate species in riparian areas are extensively discussed in the
literature (Uieda & Gajardo, 1996; Nemeth, 1998; Kikuchi & Uieda, 2005). Thus, two hypotheses may
explain the great colonization in current habitats: 1) the abundance of such in that environment is due to
Acta Scientiarum. Biological Sciences, v. 41, e45872, 2019
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Camargo et al.
the plenty amount of oxygen and food; 2) faster colonization in this environment occurs due to the drift
process, where the aquatic organisms detach themselves from the substrate to which they were attached
and attach themselves to a new underwater substrate below (Merritt & Cummins, 1996).
According to Strixino and Trivinho-Strixino (2006), many benthic invertebrates are detritivores, feeding
on organic matter produced in the water column. The accumulation of debris gives the aquatic invertebrates
a great amount of food resources and when present in satisfactory quantity it can become attractive to
benthic fauna (Rosenberg & Resh, 1982; Merrit & Cummins, 1996).
Thus, benthic invertebrates present great importance in these ecosystems, serving as a link between the
basal resources (debris and algae) and fish and crustaceans, participating in the energy flow and the cycling
of the nutrients (Bueno, Bond-Buckup, & Ferreira, 2003; Carvalho & Uieda, 2004). Therefore, knowledge on
the community structure is a fundamental step in understanding the agreement of interspecific relations
and the ecosystem as a whole (Molozzi, Salas, Callisto, & Marques, 2013), being important in the evaluation
and conservation of freshwater systems (Jiang, Xiong, Xie, & Chen, 2011).
Conclusion
We concluded that the use of natural and artificial substrates is efficient for the sampling and
colonization of the groups of aquatic invertebrates in tropical streams, being an important tool for
ecological studies. In addition, artificial substrates provide a high heterogeneity of habitat, which is able of
supporting species composition similar to the natural substrate. In the evaluation of the ecological
succession, it was not possible to observe a pattern that described the process, since the composition was
practically constant throughout the study period.
Acknowledgements
We thank Dr. Huilquer Francisco Vogel for help in the production of the map.
References
Aburaya, F. H., & Callil, C. T. (2007). Variação temporal de larvas de Chironomidae (Diptera) no Alto Rio Paraguai
(Cáceres, Mato Grosso, Brasil). Revista Brasileira de Zoologia, 24(3), 565-572. doi: 10.1590/S010181752007000300007
Anjos, A. F. d., & Takeda, A. M. (2005). Colonização de Chironomidae (Diptera:Insecta) em diferentes tipos de
substratos artificiais. Acta Scientiarum Biological Sciences, 27(2), 147-151. doi:
10.4025/actascibiolsci.v27i2.1325
Armitage, P. D., Pinder, L. C., & Cranston, P. (Eds.). (1995) The Chironomidae: the biology and ecology of nonbiting midges. Berlim, Alemanha: Springer.
Bagatini, Y. M., Delariva, R. L., & Higuti, J. (2012). Benthic macroinvertebrate community structure in a stream of
the north-west region of Paraná State, Brazil. Biota Neotropica, 12(1), 307-317. doi: 10.1590/S167606032012000100023
Bouchard Jr., R. W. (2004). Guide to aquatic invertebrates of the Upper Midwest. Identification manual for students,
citizen monitors, and aquatic resource professionals. Minneapolis, MN: University of Minnesota.
Braccia, A., Eggert, S. L., & King, N. (2014). Macroinvertebrate colonization dynamics on artificial substrates
along an algal resource gradient. Hydrobiologia, 727(1), 1-18. doi: 10.1007/s10750-013-1779-z
Brower, J. E., & Zar, J. H. (1984). Field and laboratory methods for general ecology. Dubuque, IA: W.C. Brown
Publishers.
Bueno, A. A. P., Bond-Buckup, G., & Ferreira, B. D. P. (2003). Estrutura da comunidade de invertebrados
bentônicos em dois cursos d´água do Rio Grande do Sul, Brasil. Revista Brasileira de Zoologia, 20(1), 115-125.
doi: 10.1590/S0101-81752003000100014.
Carvalho, E. M., & Uieda, V. S. (2004). Colonização por macroinvertebrados bentônicos em substrato artificial e
natural em um riacho da serra de Itatinga, São Paulo, Brasil. Revista Brasileira de Zoologia, 21(2), 287-293. doi:
10.1590/S0101-81752004000200021
Casey, R. J., & Kendall, S. A. (1996). Comparisons among colonization of artificial substratum types and natural
substratum by benthic macroinvertebrates. Hydrobiologia, 341(1), 57-64. doi: 10.1007/BF00012303
Acta Scientiarum. Biological Sciences, v. 41, e45872, 2019
Colonization of benthic invertebrates on substrates
Page 9 of 10
Dajoz, R. (1973). Ecologia Geral. Petrópolis, RJ: Vozes.
Delonzek, E. C., & Krawczyk, A. C. d. D. B. (2016). A interferência da sazonalidade sobre os grupos funcionais
tróficos de invertebrados bentônicos presentes em substrato rochoso no Rio Palmital, União da Vitória – PR.
Biotemas, 29(3), 29-34. doi: 10.5007/2175-7925.2016v29n3p29
Entrekin, S. A., Wallace, J. B., & Eggert, S. L. (2007). The response of Chironomidae (Diptera) to a long-term
exclusion of terrestrial organic matter. Hydrobiologia, 575(1), 401-413. doi: 10.1007/s10750-006-0386-7
Gotelli, N. J., & Colwell, R. K. (2001). Quantifying biodiversity: procedures and pitfalls in the measurement and
comparison of species richness. Ecology Letters, 4(4), 379-391. doi: 10.1046/j.1461-0248.2001.00230.x
Jiang, X., Xiong, J., Xie, Z., & Chen, Y. (2011). Longitudinal patterns of macroinvertebrate functional feeding
groups in a Chinese River system: a teste for river continuum concept (RCC). Quaternary International, 244(2),
289-295. doi: 10.1016/j.quaint.2010.08.015
Kikuchi, R. M., & Uieda, V. S. (2005). Composição e distribuição dos macroinvertebrados em diferentes substratos
de fundo de um riacho no município de Itatinga, São Paulo, Brasil. Entomología y Vectores, 12(2),193-231. doi:
10.1590/S0328-03812005000200006
Lisboa, L. K., Silva, A. L. L., & Petrucio, M. M. (2011). Aquatic invertebrate’s distribution in a freshwater coastal
lagoon of southern Brazil in relation to water and sediment characteristics. Acta Limnologica Brasiliensia,
23(2), 119-127. doi: 10.1590/S2179-975X2011000200002
Lovell, J. A., Fletcher, D. E., Cooper, S., & McArthur, J. V. (2017). Fish predation and macroinvertebrate
abundance on snags in low-gradient blackwater streams. Freshwater Science, 36(3), 626-634. doi:
10.1086/693474
McCafferty, W. P. (1983). Aquatic entomology: the fishermen’s and ecologists illustrated guide to insects and their
relatives. Burlington, MA: Jones & Bartlett Learning.
Merrit, R. W., & Cummins, K. W. (1996). An introduction to the aquatic insects of North America. Dubuque, IA:
Kendall / Hunt Publishing Company.
Molozzi, J., Salas, F., Callisto, M., & Marques, J. C., (2013). Thermodynamic oriented ecological indicators:
Application of Eco-Exergy and Specific Eco-Exergy in capturing environmental changes between disturbed
and non-disturbed tropical reservoirs. Ecological Indicators, 24(1), 543-551. doi: 10.1016/j.ecolind.2012.08.002
Mugnai, R., Nessimian, J. L., & Baptista, D. F. (2010). Manual de identificação de Macroinvertebrados aquáticos do
Estado do Rio de Janeiro. Rio de Janeiro, RJ: Technical Books.
Nemeth, R. S. (1998). The effect of natural variation in substrate architecture on the survival of juvenile bicolor
damselfish. Environmental Biology of Fishes, 53(2), 129-141. doi: 10.1023/A:1007402104047
Oksanen, J., Blanchet, F. G., Friendly, M., Kindit, R., Legendre, P., McGlinn, D., … Wagner, H. (2019). R package
version 2.4-0 [online]. Vegan: Community Ecology Package. Retrieved on January 15, 2019 from https://cran.rproject.org/web/packages/vegan/index.html
Pereira, D., Mansur, M. C. D., Volkmer-Ribeiro, C., Oliveira, M. D. d., Santos, C. P. d., & Bergonci, P. E. A. (2010).
Colonização de substrato artificial por macroinvertebrados límnicos, no delta do rio Jacuí (RS, Brasil). Revista
Biotemas, 23(1), 101-110. doi: 10.5007/2175-7925.2010v23n1p101
R Development Core Team. (2016). R: a language and environment for statistical computing [online]. Vienna: R
Foundation for Statistical Computing.
Rezende, C. F. (2007). Estrutura da comunidade de macroinvertebrados associados ao folhiço submerso de
remanso e correnteza em iguarapés da Amazônia Central. Biota Neotropica, 7(2), 301-305. doi: 10.1590/S167606032007000200034
Ribeiro, L. O., & Uieda, V. S. (2005). Estrutura da comunidade de macroinvertebrados bentônicos de um riacho de
serra em Itatinga, São Paulo, Brasil. Revista Brasileira de Zoologia, 22(3), 613-618. doi: 10.1590/S010181752005000300013
Rocha, L. G., Medeiros, E. S. F., & Andrade, H. T. A. (2012). Influence of flow variability on macroinvertebrate
assemblages in an intermittent stream of semi-arid Brazil. Journal of Arid Environments, 85, 33-40. doi:
10.1016/j.jaridenv.2012.04.001
Rodríguez, S. E., Becares, E., Soto, F., & Pacho, R. (1998). Colonization of aquatic macroinvertebrates in a high
mountain stream using artificial substrates. Internationale Vereinigung für Theoretische und Angewandte
Limnologie Verhandlungen, 26(3), 1120-1224. doi: 10.1080/03680770.1995.11900894
Acta Scientiarum. Biological Sciences, v. 41, e45872, 2019
Page 10 of 10
Camargo et al.
Rosenberg, D. M., & Resh, V. H. (1982). The use of artificial substrates in the study of freshwater benthic
macroinvertebrates. In J. Cairns Jr. (Ed.), Artificial Substrates (p. 175-236). Michigan, MI: Ann Arbor Science.
Santos, L. B. d., Bruno, C. G. C., & Santos, J. C. (2016). Colonization by benthic macroinvertebrates in two
artificial substrate types of a Riparian Forest. Acta Limnologica Brasiliensia, 28, e24. doi: 10.1590/s2179975x3616
Silveira Neto, S., Nakano, O., Barbin, D., & Villa Nova, N. A. (1972). Manual de ecologia dos insetos. São Paulo, SP:
Agronômica Ceres.
Simpson, G. L. (2018). Permute: functions for generating restricted permutations of data [online]. R Package, version
0.7-0. Retrieved on January 15, 2019 from https://cran.rproject.org/web/packages/permute/index.html
Statsoft inc. (2005). Statistica for Windows: data analysis software system. Version 7.1 [software]. Tulsa: Statsoft
Inc. Retrieved on January 15, 2019 from http://www.statsoft.com
Statzner, B. (1981). The relation between hydraulic stress and microdistribution of benthic macro invertebrates in
a lowland running water system, the Schierenseebrooks North Germany. Archiv fuer Hydrobiologie, 91(2), 192218.
Strixino, G., & Trivinho-Strixino, S. (2006). Herpobentos e haptobentos de lagoas marginais da Estação Ecológica
de Jataí (Luiz Antônio, SP). In: J. E. d. Santos, J. S. R. Pires & L. E. Moschini, (Eds.), Estudos Integrados em
Ecossistemas: Estação Ecológica de Jataí (Volume 3, p. 45-60). São Carlos, SP: Edufscar.
Talamoni, J. L. B., Silva, F. L., Pauleto, G. M., & Ruiz, S. S. (2009). Categorização funcional trófica das
comunidades de macroinvertebrados de dois reservatórios na região Centro-Oeste do Estado de São Paulo,
Brasil. Acta Scientiarum. Biological Sciences, 31(1), 1-7.doi: 10.4025/actascibiolsci.v31i1.331
Thomazi, R. D., Kiifer, W. P., Ferreira Junior, P. D., & Sá, F. S. (2008). A sucessão ecológica sazonal de
macroinvertebrados bentônicos em diferentes tipos de atratores artificiais no rio Bubu, Cariacica, ES.
Natureza online, 6(1), 1-8.
Trivinho-Strixino, S. (2011). Chironomidae (Insecta, Diptera, Nematocera) do Estado de São Paulo, Sudeste do
Brasil. Biota Neotropica, 11(1), 675-684. doi: 10.1590/S1676-06032011000500032
Trivinho-Strixino, S., & Sonada, K. C. (2006). A new Tanytarsus species (Insecta, Diptera, Chironomidae) from
São Paulo State, Brazil. Biota Neotropica, 6(2),1-9. doi: 10.1590/S1676-06032006000200020
Trivinho-Strixino, S., & Strixino, G. (1995). Larvas de Chironomidae (Diptera) do Estado de São Paulo: Guia de
identificação e diagnose dos gêneros. São Carlos, SP: PPG-ERN/Ufscar.
Tundisi, J.G.; & Tundisi, T.M. (2008). Limnologia. São Paulo, SP: Oficina de Textos.
Uieda, V. S., & Gajardo, I. C. S. M. (1996). Macroinvertebrados perifíticos encontrados em poções e corredeiras de
um riacho. Naturalia, 21, 31-47.
Vieira, S. (1980). Introdução à bioestatística. Rio de Janeiro, RJ: Campus.
Weber, C. I. (1973). Biological field and laboratory methods for measuring the quality of surface water and effluents.
Cincinati, OH: NERC/EPA.
Whitton, B. A. (1975). River ecology (Vol. 2). Berkeley, CA: University of California Press.
Acta Scientiarum. Biological Sciences, v. 41, e45872, 2019