Microteaching on terms used in filtration .Pharmaceutical Engineering
Artigo_Bioterra_V23_N1_07
1. REVISTA DE BIOLOGIA E CIÊNCIAS DA TERRA ISSN 1519-5228
Volume 23 - Número 1 - 1º Semestre 2023
COLONIZATION DYNAMICS OF BENTHIC MACROINVERTEBRATES IN A
BRAZILIAN SEMIARID TEMPORARY DAM
Artur Henrique Freitas Florentino de Souza¹, Martin Lindsey Christoffersen2
; Francimário da Silva Feitosa3
ABSTRACT
The community of limnic benthic invertebrates contains a diverse set of taxonomic groups, many visible to the
naked eye, living associated or not to the substrate. In order to understand the colonization of invertebrates to
these environments, an artificial substrate is used in order to reduce problems related to the variety of natural
substrates in the different locations studied. Furthermore, such a procedure results in more accurate predictions
than those made with traditional methods. This study aimed to record changes in species richness and abundance
of benthic macroinvertebrates during the processes of colonization and ecological succession of artificial
substrates in a temporary reservoir in Serra Branca, State of Paraíba. Sampling was performed weekly in the
Jatobá Dam during the rainy season (April to June, 2007), using 32 polyethylene baskets, each containing 1 kg of
artificial substrate composed of granitic gravel. Each week water samples were also collected to determine the
physical and chemical variables (temperature, pH, depth and transparency of water, conductivity, alkalinity, total
hardness of water and dissolved oxygen). These were correlated with the biological data (taxa and abundances).
We recorded a maximum richness of 37 taxa, mainly Insecta, Gastropoda, Annelida and Crustacea. There was
alternating dominance among Conchostraca, Oligochaeta and Planorbidae. Although frequent, the chironomid
flies were not dominant during the colonization process. In the eighth week of installation of the artificial
substrate, the highest means of individuals and taxa were recorded, indicating from then on, an adequacy of
relationships in the community, in terms of ecological succession, and consequent approximation to the climax
stage.
Keywords: Artificial substrate, Zoobenthos, Limnology, Caatinga Domain.
DINÂMICA DA COLONIZAÇÃO DE MACROINVERTEBRADOS BENTÔNICOS NUM
AÇUDE TEMPORÁRIO DO SEMIÁRIDO BRASILEIRO
RESUMO
A comunidade de invertebrados bentônicos límnicos contém um conjunto diversificado de grupos taxonômicos,
que podem, aparentemente, ser visíveis a olho nu, vivendo ou não presos ao substrato. No entanto, para entender a
colonização desses invertebrados nos ambientes, um substrato artificial é utilizado como forma de diminuir os
problemas relacionados à variedade de substratos naturais nas diferentes localidades estudadas. Além disso, esta
técnica resulta em previsões mais precisas do que aquelas feitas com métodos tradicionais. Este estudo teve como
objetivo registrar mudanças na riqueza e abundância de espécies de macroinvertebrados bentônicos durante os
processos de colonização e sucessão ecológica de substratos artificiais em um reservatório temporário em Serra
Branca, Estado da Paraíba. As amostragens foram realizadas semanalmente na represa Jatobá durante o período
chuvoso (abril a junho de 2007), utilizando 32 cestas de polietileno, cada uma contendo 1 kg de substrato artificial
composto de cascalho granítico. A cada semana também foram coletadas amostras de água para determinação das
variáveis físicas e químicas (temperatura, pH, profundidade e transparência da água, condutividade, alcalinidade,
dureza total da água e oxigênio dissolvido). Estes foram correlacionados com os dados biológicos (táxons e
abundâncias). Registramos uma riqueza máxima de 37 táxons, principalmente Insecta, Gastropoda, Annelida e
Crustacea. Houve dominância alternada entre Conchostraca, Oligochaeta e Planorbidae. Apesar de frequentes, os
quironomídeos não foram dominantes durante o processo de colonização. Na oitava semana de instalação dos
substratos, foram registradas as maiores médias de indivíduos e táxons, indicando a partir de então uma adequação
das relações na comunidade, em termos de sucessão ecológica, e consequente aproximação do estágio clímax.
Palavras-chaves: Substrato artificial, Zoobentos, Limnologia, Caatinga.
80
2. 1. INTRODUCTION
The community of benthic invertebrates
of continental waters contains a diverse
assemblage of taxonomical groups. For
example, there are crustaceans, mollusks,
annelids and adult or immature insects.
Individuals usually exceed 0.2mm (Henry,
2003). Such a biotic community is fundamental
in rivers and lakes for the bioturbation of
sediments and for the consequent turnover of
organic matter (MARQUES et al., 1999).
The main factors for the successful
establishment of zoobenthic communities are
habitat quality (MARQUES et al., 1999) and
physical conditions such as geomorphology,
current velocity, flow rate, substrate type and
retention time. All these factors decisively
influence the colonization and the successional
dynamics of these communities (CARVALHO;
UIEDA, 2004). These animals have a large
presence in lentic ecosystems, being
preferentialy found in the costal zone, whose
characteristics favor the development of their
community (BUTAKKA et al., 2014)
Artificial substrates are artefacts that try to
mimic environmental characters. They contain
substrates that are auspicious for the
colonization of benthic organisms. These
artefacts have been largely used, in a
standardized way, as a means of reducing
problems related to the variety of natural
substrates in the different studied localities.
They are thus considered an important tool for
monitoring water bodies and/or for measuring
the degradation of aquatic continental
ecosystems (BICUDO; BICUDO, 2004).
According to these same authors, the use of
artificial substrates as an environmental tool
results in more accurate predictions than those
made with traditional methods. Thus, there are
more guarantees for the elaboration of efficient
strategies for the management and conservation
of continental aquatic systems and for the
monitoring of different water bodies.
Colonization experiments permit us to
know the invertebrate fauna present in a certain
area. They also enable the analysis of the
temporal changes that affect the zoobenthic
community composition due to natural or
stochastic processes (e.g., anthropogenic);
consequently, these groups are largely used in
studies that aim at environmental bioindication
(CARVALHO, UIEDA, 2004). Another
important aspect in the use of artificial
substrates is the possibility of evaluating the
successional stages of zoobenthos in the area
(Santos et al., 2016).
The main aim of this study is to analyze
changes in the taxonomic richness, frequency
and abundance of benthic invertebrates during
the process of colonization and ecological
succession of these animals in artificial
substrates. The collections took place in the
rainy season in the Municipality of Serra
Branca, State of Paraíba. The period in which
the water blade is present in the Jatobá Dam is
short.
2. MATERIAL AND METHODS
2.1 Study Area
The municipality of Serra Branca is
located in the geo-environmental unit of the
Borborema plateau, in the State of Paraíba,
Brazil. It is situated in the domain of the river
Taperoá sub-basin, an hydrographic basin of the
Paraíba River (BRASIL, 2005). The area of the
unit is crossed by permanent rivers,
notwithstanding with a low flow rate. The
potential for subterranean water is low and the
vegetation of the municipality is formed by
semideciduous and deciduous forests, typical of
the Caatinga Domain. The climate is of the
Tropical Rainy type, with a dry summer.
The Jatobá Dam (Figure 1) is filled in the
rainy season by a stream of the same name. Its
geographical coordinates are 7º 29’ 41.27’’S,
36º 44’ 03.06’’W. It is located 534 m above sea
level.
3. Figure 1. Jatobá Dam, at the municipality of Serra
Branca, Paraíba, in the rainy season (A) and dry season
(B); Polyethylene baskets, containing 1 kg of granite
gravel as an artificial substrate (C). Source: produced by
the authors.
The reservoir measures 330m in length
and 168m in width, being up to 2.5 m deep. This
small hydraulic basin is of a temporary nature.
Both swimming and fishing with the use of nets
is prohibited.
2.2 Environmental and biological variables
The data for the rainfall of the region, in
millimeters (mm), were obtained at the Empresa
de Assistência Técnica e Extensão Rural
(EMATER) of Serra Branca. These data were
collected with a pluviometer with a precision of
0.1mm, placed in an open space of 20m2
,
without obstacles, 1.5 m above the ground.
Measurements were made daily, always at 7:00
A.M.
Among Physical and Chemical Variables
of the Water, samples of surface water were
collected in the same day, hour and place of the
artificial substrates. These were immediately
transported in a thermal box with ice in order to
lower photosynthesis, respiration and
decomposition of the organisms in the water. In
the lab, they were transferred to a freezer, where
they remained until processing.
Variables determined in the lab were:
Electric Conductivity (µS.cm-1
), with the use of
a conductive meter; Alkalinity (mg CaCO3.L-1
)
determined by titration, following the method
described in Standard Methods (Eaton et al.,
1995); Total Water Hardness (mg CaCO3.L-1
)
determined by titration, also following the
method described in Standard Methods (Eaton
et al., 1995); and Dissolved Oxygen (mg O2.L-1
)
determined by the classic method of Winkler
(GOLTERMAN et al., 1978).
The experimentation with colonization
and ecological succession of the zoobenthos
occurred during the period from March to May,
2007 (rainy season), totaling 10 (ten) weeks.
From the second week of installation three
samples were collected weekly at the same pre-
established time, always at 9 a.m.
Thirty-two polyethylene baskets with openings
of 1.5cm x 1.5cm, were used. Each one (a total
capacity of 2000 cm3
– Figure 1C) was filled
with 1kg of granitic gravel to serve as the
artificial substrate; they were placed
equidistantly 2m apart and at a mean depth of
90 cm, and their position was marked by a
strand of styrofoam. The physical and chemical
variables of the water samples were measured
before the submersion of the artificial substrates
(W0, March 17).
After 15 days of substrate installation,
three substrates were collected in a random way.
This procedure was repeated during nine weeks,
being labeled as: W2 (March 31), W3 (April
07), W4 (April 14), W5 (April 21), W6 (April
28), W7 (May 05), W8 (May 12), W9 (May 19)
and W10 (May 26).
The baskets were rescued using a delta
sieve with a mesh of 500 µm, placed in black
plastic bags containing crystals of menthol,
without the presence of fixatives of
preservatives, and maintained in styrofoam
boxes with ice. The bags were transported to the
lab, where the animals were separated in white
plastic trays with the help of bright lamps.
The obtained animals were fixed and
preserved in absolute alcohol. Later, the
samples were preserved in alcohol at 70%.
Benthic organisms were identified with the help
of a Zeiss stereomicroscope and with
specialized identification keys (MERRIT;
CUMMINS, 1984; EPLER, 2006, 2010;
MUNGAI et al., 2010), as well as further
specialized literature.
Regarding data analysis, the Shapiro-Wilk
test was applied to verify the normality of the
abiotic data. As data did not follow a normal
pattern, non-parametric tests were applied.
The U test of Man-Whitney was used to
compare organism abundance with the
correlation index of Spearman. These tests were
calculated with the software Statistica for
Windows (STATSOFT, 2004).
3. RESULTS
3.1. Environmental Variables
The rainfall accumulated during the
period of the experiment was 188.12 mm. The
highest weekly values occurred during the
installation of the substrates (41.1mm), sixth
and seventh week (47.6 and 41.7 mm,
4. respectively). It did not rain during the third
week during substrate retrieval (W3) (Figure 2).
Figure 2 – Weekly rainfall (mm) at the Municipality of
Serra Branca, Paraíba, during the months of March to
May, 2007.
Regarding water transparency, deepest
values were obtained during their installation
(W0), with 92.66 cm. The smallest value was
obtained at W4, with 45.33 cm (Figure 3A); the
mean depth of the artificial substrates followed
due to the low depth of this aquatic system.
Figure 3. Mean values Water Transparency (A), pH (B),
Dissolved Oxygen (C), Temperature (D), Alkalinity (E),
Electric Conductivity (F) and Total Water Hardness (G),
of artificial substrates and in Jatobá Dam, Serra Branca,
Paraíba, during the months of March to May, 2007 (rainy
season). Source: Research Data.
The mean values of pH remained slightly
acid during the entire experiment, with
minimum and maximum values varying from
5.5 (W2) to 7.1 (W9). The mean variation of pH
in the Jatobá Dam was 0.9 (Figure 3B).
A moderate variation in the mean
dissolved oxygen content was observed during
the months of the experiments, with a span of
2.0 mg O2.L-1
(Figure 3C). The mean water
temperature remained above 24ºC, however the
highest mean value occurred in W3, with
27.3ºC. (Figure 3D). Mean alkalinity values
(Figure 3E) remained very low, with a
conspicuous variation between W2 and W3.
The mean values of electric conductivity
(Figure 3F) showed strong oscillations during
the duration of the experiment, with a difference
of 96.9 µS.cm-1
. Regarding the means of total
water hardness, these had little temporal
variation, a difference of 7 mg CaCO3.L-1
being
recorded (Figure 3G).
3.2. Zoobenthos and the Artificial Substrates
We counted 32 taxa in the zoobenthos,
represented by: Gastropoda (Physidae,
Planorbidae, Ancylidae), Insecta (Coleoptera,
Diptera, Heteroptera, Neuroptera, Odonata,
Ephemeroptera), Crustacea (Ostracoda and
Conchostraca), Platyhelminthes, Cnidaria
(Hydrozoa), Annelida (Oligochaeta and
Hirudinea), Nematomorpha and Hydracarina
(Table 1).
The mean of the total individuals
collected and taxon richness were most
expressive during the eighth week after the
installation of the substrates (W8), with 781
organisms and 21 taxa recorded, respectively.
In W6, 640 organisms were recorded as the
mean total of benthonic macroinvertebrates,
even though only 12 taxa were present, the
lowest richness recorded in the entire study.
Regarding the dynamics of colonization of
the substrates, we recorded changes in the
dominance by three taxa: 1) Conchostraca in
W2, with 28.5%, and W3, with 37.1%, but in
W7 these crustaceans presented the largest
number of specimens (mean of 130 individuals),
and then decreasing their numbers during the
remaining weeks; 2) the mollusk Biomphalaria
sp. was dominant mainly in W4 and W7, with
45.5% and 27.9%, respectively. These
planorbids contributed with a relative
abundance above 20% during all weeks of the
5. experiment; and 3) the Oligochaeta dominated
in W7 (42.6%) and W9 (38.3%), with the
highest mean percentage recorded, 50.1%
during the uninstallation week of the experiment
(W10), as shown in Table 01 (Figure 4).
Table 1. Mean richness of taxa, abundance and relative
frequency of the benthic macroinvertebrates obtained
during experiments with artificial substrates in Jatobá
Dam (Serra Branca, Paraíba), along the months of April
to June, 2007, corresponding to the rainy season.
Source: Research Data.
Figure 4. Mean zoobenthos dynamics during the
colonization of artificial substrates in the temporary
Jatobá Dam, during the months of March to May, 2007.
Source: Research Data.
Diptera belonging to Chironomidae were
also expressive, having a maximum recorded
frequency of 17.1% in W1, showing their
numerical importance among the insects as
pioneers in the colonization of the artificial
substrates. However, their abundance decreased
at the end of the experiment, 4.4% being
recorded in W9. Hydra iheringi was recorded
beginning in the third week of the experiment
(W3), attaining a mean relative abundance of
8.3% in W5 and then disappearing in W7 and
beyond.
The correlations of Spearman among the
environmental variables and the biological data
showed significant correlations among rainfall
and the number of hydras (r = 0.53; p < 0.05),
electric conductivity and the numbers of
Oligochaeta (r = 0.78; p < 0.05) and total
individuals and electric conductivity (r = 0.55;
p < 0.05).
4. DISCUSSION
Environmental factors such as rainfall and
changes in the physical and chemical properties
of the water may have influenced our results.
According to Abílio (2006) and Souza, Abílio
(2006), environmental factors such as rainfall
induce changes in the physical, chemical, and
biological characteristics of aquatic systems,
particularly in temporary environments in the
semiarid region of Brazil.
During the experiment, some
environmental variables such as mean alkalinity
and water hardness showed relatively low
values, when compared to other reservoirs in the
region. This may be explained by the rains
occurring in the municipality of Serra Branca
and by the great quantity of crystalline rocks
present in the micro-basin, which is located in a
zone of igneous rock (BRASIL, 2005). Other
factors, such as soil type present in the hydric
basin and in the basin of the Jatobá River may
also have contributed to the low levels of the
mentioned variables, which were previously
influenced directly by the conditions of the
Jatobá Hill range.
The mean pH values were slightly acid,
which may be explained by the probably
dystrophic condition of the environment, as
indicated by the brownish-yellowish color of the
water. According to Esteves (2011), most
continental hydraulic basins present pH values
oscillating between 6.0 and 8.0. Corroborating
this idea, Girardi et al. (2016) said that water
quality is influenced by river flow, where it is
understood that the geological nature of basin in
which a hydraulic body is situated may
6. influence the changes in pH, as well as of the
Electric Conductivity.
Even with acid pH and water Hardness
not so high, with soft water classification
(WHO, 2017), these variables were not enough
to limit the presence of molluscs such as
Glundachia sp., Drepanotrema sp. and, in
particular, the expressive abundance and
frequency of the gastropods Biomphalaria sp.
throughout the experiment, since they need
CaCO3 for the composition of the shell. Such
molluscs are very common in the aquatic
environments of the Caatinga (KOTZIAN;
AMARAL, 2013).
Regarding the macroinvertebrates, insects
were the most frequent in the colonization of the
artificial substrates. According to Correia and
Trivino-Strixino (2005), most aquatic insects
are intimately associated with the substrate, at
least during a phase of their life cycle. In the
present study, chironomid larvae were most
representative during the first week of the
experiment (W1), being considered important
pioneers in the colonization of new aquatic
substrates (SILVA, Henry, 2017). In fact, the
substrate exerts a great influence on these
animals. It may affect the growth and survival
directly, as the substrate provides the habitat, its
food, and protection. According to the results
obtained by Carvalho, Uieda (2004), Ribeiro,
Ueda (2006), and Souza et al. (2008), whom
also used the process of colonization of artificial
substrates, the assemblage of chironomids was
dominant. In this study, on the other hand, this
taxon did not become dominant at any moment
during the nine weeks during which the
experiment was conducted, even though it was
the most expressive among insects during the
first week (W1), corroborating the results of
Silva et al. (2016). These authors showed that in
their experiments of colonization with artificial
substrates Chironomidae are dominant in
periods of drought.
The dominance of oligochaetes in the
Jatobá Dam, from W10, W6 and W5 onwards,
may be explained on the basis of the results of
Silva et al. (2016) and Silva, Henrt (2017), also
based on artificial substrates. These authors
found that annelids become dominant in the
rainy season. In W6, however, there was a lower
taxonomic richness and a dominance of
Oligochaeta, associated with a low abundance
of predatory taxa such as Odonata, Ditiscidae,
Heteroptera and Hirudinea, coinciding with the
highest rainfall accumulated during that week.
According to Oricchio, Flores, Dias (2016),
predation can alter the composition, richness
and abundance of substrate-colonizing
communities.
Regarding Ostracoda, Monkolski (2006)
finds that this typical benthic group is tolerant to
stress from low oxygen content and may even
become abundant under these conditions. On the
other hand, Souza, Abílio (2006) find that
Ostracoda are usually common in temporary
environments, being strongly affected by
oxygen content and water temperature.
In contrast to other studies in aquatic
water bodies in the basin of the Taperoá River,
the exotic thiarid gastropod Melanoides
tuberculata (Müller, 1774) was not recorded in
our study. This Afro-Asiatic species, which is
resistant to desiccation and has a pandemic
distribution (Pamplim & Rocha, 2005), is also
found in several water bodies in the semiarid
region of the Paraíba State (ABÍLIO et al.,
2006, 2007; Santana et al., 2009; KOTZIAN;
AMARAL, 2013). According to Pamplim,
Rocha (2005), the recording of this species
worldwide indicates a strong and rapid
dispersal, the species being introduced into
several environments as a biological regulator
against Biomphalaria sp., the intermediary host
of Schistosoma mansoni Sambon, 1907, which
provokes Schistosomiasis. In fact, the absence
of M. tuberculata in our study would explain the
high frequency of Biomphalaria sp. in the
studied zoobenthic community.
On the other hand, Souza et al. (2008),
using the same methods, recorded a low
frequency of Biomphalaria sp. in the
colonization of the public reservoir of Jatobá I,
in Patos, Paraíba State. This suggests that the
presence of M. tuberculata directly influenced
the population of the planorbid Biomphalaria
sp. Guimarães et al. (2001) recorded similar
results in two lagoons in Belo Horizonte, Minas
Gerais State, where the presence of M.
tuberculata appears to have reduced the
populations of Biomphalaria sp.
Finally, the colonization os zoobenthos in
stony articifical substrates proved to be an
excellent tool to analyse the dynamics of the
colonization of the limnic zoobenthos,
7. presenting in the final weeks of the experiment
the highest species richness, with Conchostraca,
Ostracoda and Chironomidae being the
pioneers, while Oligochaeta and gastropods
Biomphalaria sp. Were the most frequent.
ACKNOWLEDGMENTS
Prof. Dr. Francisco José Pegado Abílio,
from Departamento de Metodologia da
Educação/Centro de Educação, Universidade
Federal da Paraíba, Campus I, provided logistic
help. João, from EMATER of Serra Branca,
Paraíba State, provided the pluviometric data
for the studies in the Municipality of Serra
Branca, Paraíba State.
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______________________________________
1. Departamento de Sistemática e
Ecologia, Universidade Federal da
Paraíba - UFPB, Cidade Universitária I,
900, CEP 58059-900, João Pessoa, PB,
Brasil; e-mail: ahffs@ccen.ufpb.br
ORCID: https://orcid.org/0000-0002-
9069-7950
2. Departamento de Sistemática e Ecologia,
Universidade Federal da Paraíba -
UFPB, Cidade Universitária I, 900, CEP
58059-900, João Pessoa, PB, Brasil; e-
mail: martinlc.ufpb@gmail.com
ORCID: https://orcid.org/0000-0001-
8108-1938
3. Colegiado de Ciências da Natureza,
Universidade Federal do Vale do São
Francisco - UNIVASF, Campus Serra
da Capivara, Rua João Ferreira dos
Santos s/n, Bairro Campestre, CEP
64770-000, São Raimundo Nonato, PI,
Brasil; e-mail:
francimario.feitosa@univasf.edu.br
ORCID: https://orcid.org/0000-0002-
8463-3707
88