You are on page 1of 21

See

discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/284246366

Microzooplankton as a bioindicator of
environmental degradation in the Amazon

Article in Ecological Indicators · November 2015


DOI: 10.1016/j.ecolind.2015.10.005

CITATIONS READS

2 62

4 authors, including:

Brenda Costa Marcelo de O. Lima


Instituto Evandro Chagas Evandro Chagas Institute
2 PUBLICATIONS 3 CITATIONS 29 PUBLICATIONS 98 CITATIONS

SEE PROFILE SEE PROFILE

All content following this page was uploaded by Brenda Costa on 30 November 2016.

The user has requested enhancement of the downloaded file. All in-text references underlined in blue are added to the original document
and are linked to publications on ResearchGate, letting you access and read them immediately.
Ecological Indicators 61 (2016) 526–545

Contents lists available at ScienceDirect

Ecological Indicators
journal homepage: www.elsevier.com/locate/ecolind

Microzooplankton as a bioindicator of environmental degradation in


the Amazon
Brenda Natasha Souza Costa a,b,∗ , Samara Cristina Campelo Pinheiro b ,
Lílian Lund Amado a , Marcelo de Oliveira Lima a,b
a
Postgraduate Program in Aquatic Ecology and Fish, Federal University of Pará, Brazil
b
Evandro Chagas Institute, Brazil

a r t i c l e i n f o a b s t r a c t

Article history: Recent studies have assessed the impact of the discharge of untreated domestic and industrial effluents on
Received 30 January 2015 aquatic ecosystems. In the 1980s, large industrial factories were set up in the municipality of Barcarena,
Received in revised form Amazon, Brazil; however, this was not accompanied by investments to improve basic sanitation and
29 September 2015
housing structures in the region, resulting in deterioration of the surface water quality. The main aims of
Accepted 3 October 2015
this study were to characterize the zooplankton community of surface water to elucidate the influence
Available online 19 November 2015
of unregulated territorial occupation and industrial development on ecosystem degradation of three
rivers located near the industrial and port area of Barcarena. The physico-chemical and microbiological
Keywords:
Pollution
parameters linked to water quality assessment were also analyzed. In each river, three sites were selected
River for sampling, which was performed quarterly in 2012. The zooplankton community of the three rivers
Amazon comprised 149 taxa, and the density of zooplankton varied among rivers; Arapiranga River had the lowest
Zooplankton values, followed by Curuperê-Dendê and Murucupi Rivers. IndVal analyses show that Keratella lenzi and
Anuraeopsis sp1 have elevated fidelity and specificity to the Curuperê-Dendê and Murucupi Rivers, both of
which are strongly affected by anthropogenic forces. Difflugia distenda and Difflugia sp7 were associated
with Arapiranga River, which has a well-conserved ecosystem.
© 2015 Elsevier Ltd. All rights reserved.

1. Introduction environmental degradation leading to damaging effects on the


fauna and flora of terrestrial and aquatic ecosystems in these
In the 19th century, the creation of industrial zones in several regions (Marale, 2012).
countries led to immigration to these areas and the formation of Throughout the years, many studies have been conducted glob-
urban centers with high population densities. However, this rapid ally to assess the impact of domestic and industrial effluents
population growth was not followed by the necessary investments on aquatic ecosystems. These effluents can lead to accumula-
in infrastructure in most countries, and areas located next to indus- tion of toxic substances in the abiotic environment that can
trial zones became suburbs characterized by poor basic sanitation spread to different trophic levels, resulting in death, physiologi-
and other conditions leading to a low quality of life (Maitra, 2011; cal and/or morphological changes in all organisms (Moon et al.,
Silva and Silveira, 2006). 1994; Eschenhagen et al., 2003; Rocchetta et al., 2014). One exam-
The precarious conditions of essential public services, social ple of this problem is the Mushim-chum estuary, located in the city
networks, and rapid immigration processes generate multiple of Chungiu (South Korea), affected by point sources of domestic
impacts, not restricted to human health, that extend to the envi- effluents and where metal analyses revealed concentrations of Cd,
ronment (Clark, 2005). The absence of solid waste management Pb, and Zn that were higher than in other similar areas with no
policies and insufficient sewage systems contribute decisively to anthropic activities (Moon et al., 1994). Subsequent studies using
select species as bioindicators demonstrated that changes in lipid
composition and increased oxidative stress in mollusks exposed
∗ Corresponding author at: Postgraduate Program in Aquatic Ecology and Fish, to environments contaminated with the discharge of domestic
Federal University of Pará, Brazil. sewage (Rocchetta et al., 2014). At Port Harcourt (Nigeria), an area
E-mail address: brendanatasha@biologa.bio.br (B.N.S. Costa). inundated with domestic and sanitary effluents, analysis of the

http://dx.doi.org/10.1016/j.ecolind.2015.10.005
1470-160X/© 2015 Elsevier Ltd. All rights reserved.
B.N.S. Costa et al. / Ecological Indicators 61 (2016) 526–545 527

zooplankton community showed that these microorganisms 2. Materials and methods


adapted to environments with high levels of pollution (Davies,
2009). 2.1. Study area
The same conditions were observed in the Amazon in the 1980s
when large companies were established in the Barcarena City. This The source of the Murucupi River is in an environmental preser-
was initially due to the government’s drive to implement regional vation area, bordered by the districts of Vila de Itupanema and Vila
development policies and strengthen the mineral verticalization dos Cabanos, Highway PA-483, and the (red mud) residue, tailing
process of aluminum (Pressler, 2005). After large industries set- pond of the alumina producing industrial hub. Its natural course
tled in the region, population growth quadrupled from 1980 to runs through a region with Vila dos Cabanos on its left bank, and Vila
1991, with the total number of inhabitants increasing from 20,000 do Laranjal on its right bank, finally discharging into Furo do Arrozal
to 90,000 in only one decade. This rapid population growth, with after 10 km, a channel that connects the Pará and São Francisco
the main increase in the areas surrounding the companies, was rivers. Its riparian forests have been devastated and there are large
driven by the availability of potential jobs, mainly during the ini- stripped areas next to the river sources, as well as impoundments
tial development phase of the factories (Lima, 2011). The growth for recreation. Areas for leisure are located along the entire river
in population density resulted in the creation of new districts as well as regions for subsistence fishing activities, mainly located
(Vila dos Cabanos, Bairro Industrial, and Vila do Canaã), as well near riverside dwellers along the banks (Faial, 2009). Historically,
as increase in the populations of existing ones (Vila do Laranjal there were breaches in the red mud tailing ponds in 2003 and
and Vila do Conde). However, no necessary investments to improve 2009, leading to a discharge of solid materials and alkaline efflu-
basic sanitation and housing structures corresponding to this mass ents directly into the Murucupi River. Discharge ducts or channels
population movement toward Barcarena were made in the region. of untreated domestic and sanitary effluents have been recorded
This led to a precarious infrastructure that resulted in the direct from Vila dos Cabanos and Vila do Laranjal (Santos et al., 2003;
discharge of untreated domestic and industrial effluents into the Lima et al., 2009).
local rivers, changing the quality of surface waters that had been The main sources of the Curuperê Stream are located next to
essential for subsistence fishing, leisure, and human consumption the residue tailing ponds of kaolin processing companies and, its
(Lima, 2011). natural course is characterized by traditional communities on its
Studies demonstrate that monitoring of bioindicators might left bank (quilombo). On its banks, the riparian forests have been
be ideal tools to assess the impact of effluent on the environ- devastated and there are records of discharge of industrial effluents
ment before damage reaches higher trophic levels. Bioindicators resulting from kaolin processing from 1998 to 2014 (Carneiro et al.,
are organisms that respond preventively to possible changes in the 2007; Lima, 2011; Lima et al., 2009). After 3 km from the source, this
environment (Van Gestel and Van Brummelen, 1996). Because of river flows into the Dendê stream near the community of Ilha São
their short life cycle, most planktonic microorganisms are consid- João.
ered to be excellent bioindicators of environmental changes, as they The Dendê stream begins in a preserved environmental loca-
respond quickly to shifts in the aquatic environment where they are tion, found near the industrial processing plans for the electrolytic
placed (Ji et al., 2013). Among these microorganisms, zooplankton reduction of alumina into aluminum ingot. The natural course of
play a key role in the energy transfer between primary producers this stream passes through a region with Trevo do Peteca and Vila
and higher trophic levels and respond differently to environmental do Conde on its right bank, and the communities of the Industrial
changes (Dussart, 1964). Previous studies showed that cell modifi- District, São Jorge, Ilha São João, and Vila Maricá, on its left bank.
cations (mutations) may occur in these microorganisms, as well as Before the stream eventually flows into the Pará River, approx-
changes in the density and diversity of the overall community. For imately 7 km away, it runs along another area used for kaolin
these reasons, in some cases, environmental shifts might have var- processing. The riparian forests have also been devastated in this
ious consequences on the zooplankton community leading to the region, leading to the discharge of untreated domestic and san-
disappearance of some species or to the adaptation of opportunistic itation effluents into the stream. Due to the short extensions of
species (Mclusky, 1989; Uriarte and Villate, 2004). It is well docu- the Curuperê and Dendê Streams they were grouped into a single
mented that the analysis of variation in zooplankton communities drainage referred to as the Curuperê-Dendê.
is an important tool to assess the effects of anthropic activities on The Arapiranga River begins in the city of Abaetetuba, in the
marine and freshwater aquatic systems (Moraitou-Apostolopoulou northern region of Brazil and discharges into the Pará River next to
and Ignatiades, 1980; Marneffe et al., 1996; Uriarte and Villate, Vila de Beja. Along its banks, the riparian forests are relatively pre-
2004; Jiang et al., 2010). served compared to the characteristics of other drainages nearby,
In freshwater ecosystems, the zooplankton community is such as the Murucupi River, the Curuperê stream, and the Dendê
comprised predominantly of organisms belonging to the Clado- stream, mentioned above. Due to these peculiar characteristics,
cera, Copepoda (Cyclopoida and Calanoida), Rotifera, and Protista which indicate that it is well environmentally preserved, and since
(Heerkloss and Schnese, 1999). In environments affected by human it is located farther from the industrial and port areas of Barcarena
activity, there is an increase in abundance of Cladocera, Rotifera, with no sewage or industrial effluent discharges recorded on its
and Cyclopoida, while Calanoida is more suited to oligotrophic banks, the Arapiranga River was used as a the control river for this
environments and is not detected after the environment shows study.
signals of eutrophication (Perbiche-Neves et al., 2013). Neverthe-
less, there are records showing that the density and composition
of these groups might be affected by regional climate change that 2.2. Regional climatic characteristics
influences the exchange of nutrients between the terrestrial and
aquatic environments (Etilé et al., 2008). Seasonal rainfall is characterized by a rainy season, typically
The main aim of this study was to characterize the zooplankton running from November through April, and a less rainy season, run-
community in order to assess the influence of unmanaged terri- ning May through October (INMET, 2014; Moraes et al., 1998). To
torial occupation and industrial development on environmental confirm and characterize the rain flow cycle, data on monthly rain-
degradation in three rivers located near the industrial and port fall, maximum temperature, relative humidity, and wind speed in
regions of Barcarena city (Curuperê-Dendê and Murucupi rivers) the study area were obtained from the National Institute of Mete-
and its surrounding area (Arapiranga river). orology (INMET) database (Belém station).
528 B.N.S. Costa et al. / Ecological Indicators 61 (2016) 526–545

Fig. 1. Study area in the Arapiranga (A), Curuperê-Dendê (C) and Murucupi (M) rivers located in Bacarena and Abaetetuba, Pará, Brazil.

2.3. Sampling
800 8
A Precipitation
Sampling was carried out quarterly in February, May, August, 700
Wind
7
Total Precipitation (mm)

and November 2012, in order to analyze a complete annual 600 6

Wind Speed (mps)


cycle. All sampling took place during the lowest ebbing tide
500 5
(full moon). For all the rivers analyzed, the sampling stations
were defined as follows: they were distributed at the upstream 400 4
region (P1), an intermediate area (P2), and at a downstream 300 3
site (P3) (Fig. 1). Due to their short extensions the Curuperê
200 2
and Dendê streams were grouped into a single drainage called
Curuperê-Dendê, with point P1 in Dendê, and points P2 and P3 in 100 1
Curuperê. 0 0
For the physico-chemical analyses of surface waters, polypro- November
October
April

December
June
May

August
March

September
January
February

July

pylene flasks (500 mL and 1000 mL) were used. All sampling was
performed at a depth of approximately 30 cm in the water column.
For fecal coliform samples, 100-mL NASCOS® bags were used and
Month
transported in isothermal boxes.
Samples for the qualitative study of the zooplankton community
were obtained by horizontal trawling at the water column subsur- 34 95
B
face, using a plankton net with 64 ␮m mesh size. Samples for the 34
Maximum Temperature (ºC)

33 90
quantitative study were obtained by filtering 200 L of water using
33
Relative Humidity (%)

a 10 L graduated stainless steel bucket. Subsequently, the material 85


collected was fixed in a 6% formaldehyde solution (ASTM E1200- 32
32
87(2012), 2012) and stored in thermal boxes. 80
31
31
2.4. Physico-chemical and microbiological analyses 75
30
30 Temperature 70
The following variables were measured in situ: temperature
29 Humidity
(T), hydrogenionic potential (pH), electric conductivity (EC), total
29 65
dissolved solids (TDS), salinity (SAL), and dissolved oxygen (DO),
April

October
November
December
June
May

August
March

September
January
February

July

using a portable multiparameter meter (HI9828, HANNA® ), pre-


viously calibrated. Water transparency was estimated by using a
Secchi disk, with a diameter of 30 cm. The turbidity (TRB), apparent
Month
color (COLOR), total suspended solids (TSS), and chemical oxygen
demand (COD) were determined by UV–VIS spectrophotometry. To Fig. 2. (A) Total rainfall and wind speed; (B) maximum temperature and relative
obtain the biochemical oxygen demand (BOD), we used the five-day humidity in 2012.
incubation technique (APHA et al., 2012). The nitrite-N (N-NO2 − ), Source: INMET (2014).
B.N.S. Costa et al. / Ecological Indicators 61 (2016) 526–545 529

Table 1
Water Quality Index in Arapiranga, Curuperê-Dendê, and Murucupi rivers in 2012.

Rivers February May August November Mean Classification

Pt 01 Pt 02 Pt 03 Pt 01 Pt 02 Pt 03 Pt 01 Pt 02 Pt 03 Pt 01 Pt 02 Pt 03

Arapiranga 49 48 59 50 46 57 57 55 65 52 52 62 54 Good
Curuperê-Dendê 47 50 50 48 59 51 36 42 42 49 57 51 49 Fair
Murucupi 30 37 45 33 36 44 44 39 56 40 39 52 41 Fair

Table 2
Seasonal variation of physicochemical variables in the Arapiranga River in 2012.

Physico chemical variables February May August November

A1 A2 A3 A1 A2 A3 A1 A2 A3 A1 A2 A3

T (◦ C) 25.96 26.94 28.22 26.00 27.00 28.00 26.70 26.86 29.06 26.86 26.99 28.53
pH 5.13 5.50 6.41 4.94 4.18 5.84 5.50 5.45 6.63 5.45 5.35 6.40
EC (␮S cm−1 ) 18.00 20.00 39.00 14.00 17.00 26.00 18.00 16.00 40.00 26.00 27.00 72.00
TDS (mg L−1 ) 9.00 10.00 20.00 7.00 8.00 13.00 9.00 8.00 20.00 13.00 13.00 36.00
SAL (mg L−1 ) 0.01 0.01 0.02 0.00 0.01 0.01 0.01 0.01 0.02 0.01 0.01 0.03
DO (mg L−1 ) 6.60 6.79 9.36 3.92 4.34 2.53 6.12 5.45 6.40 7.81 7.19 8.39
Transparency (cm) 70.00 50.00 50.00 70.00 50.00 60.00 110.00 90.00 80.00 60.00 60.00 50.00
TRB (UNT) 27.60 14.40 19.20 6.00 8.00 8.00 20.00 23.00 23.00 16.00 15.00 18.00
COLOR (UC) 14.00 14.00 7.00 46.00 56.00 43.00 25.00 21.00 29.00 38.00 30.00 23.00
TSS (mg L−1 ) 23.00 12.00 16.00 4.00 11.00 10.00 9.00 15.00 12.00 6.00 4.00 7.00
COD (mg L−1 ) 34.00 30.00 12.00 28.00 73.00 40.00 11.00 14.00 14.00 24.00 22.00 24.00
BOD (mg L−1 ) 8.00 9.00 6.00 10.00 42.00 18.00 5.00 3.00 5.00 10.00 9.00 6.00
N-NO2 − (mg L−1 ) 0.02 0.06 0.05 0.05 0.02 0.02 0.04 0.06 0.02 0.04 0.03 0.02
N-NO3 − (mg L−1 ) 0.42 0.63 0.72 0.17 0.26 0.21 0.53 0.97 2.39 0.73 0.59 0.77
N-NH4 (mg L−1 ) 0.12 0.11 0.10 0.03 0.10 0.08 0.08 0.09 0.17 0.41 0.09 0.05
P04 3− (mg L−1 ) 0.07 0.10 0.04 0.04 0.03 0.04 0.09 0.03 0.04 0.02 0.05 0.03
SO4 2− (mg L−1 ) 1.84 1.94 1.91 0.31 0.30 0.36 0.53 0.68 1.53 1.20 1.05 1.82
F− (mg L−1 ) 2.13 2.10 1.87 0.01 0.01 0.02 0.01 0.02 0.03 0.02 0.01 0.03
Hardness (mg L−1 ) 4.93 5.02 6.97 0.88 1.51 2.58 2.28 4.77 4.64 2.58 2.64 5.69
Alkalinity (mg L−1 ) 5.00 5.00 20.00 20.00 17.50 30.00 35.00 30.00 40.00 6.00 6.00 15.00
Cl− (mg L−1 ) 2.13 2.10 1.87 1.39 1.24 1.11 1.68 1.28 4.61 1.76 1.67 1.49
NH3 (mg L−1 ) 0.10 0.09 0.08 0.03 0.08 0.07 0.07 0.08 0.14 0.34 0.07 0.04

nitrate-N (N-NO3 − ), ammonium N (N-NH4 ), ammonia (NH3 ), 2.5. Water Quality Index (WQI)
phosphate (PO4 3− ), sulfate (SO4 2− ), hardness, total alkalinity, fluo-
ride (F− ), and chloride (Cl− ) were measured by Ion Chromatography WQI values were determined according to the criteria and
(ICS DUAL 2000-DIONEX). equations set forth by the Environmental Sanitation Technol-
The most probable numbers (MPN) of fecal coliform, used to ogy Company (CETESB), Government of the State of São Paulo,
calculate the water quality index (WQI), were measured using Brazil (Von Sperling, 2009). Based on this index, the water qual-
QUANTI-TRAYS in a water bath at a constant temperature of ity was classified as poor (WQI ≤ 19), marginal (19 < WQI ≥ 36), fair
44.5 ◦ C. (36 < WQI ≥ 51), good (51 < WQI ≥ 79), or very good (WQI > 79).

Table 3
Seasonal variation of physicochemical variables in the Curuperê-Dendê River in 2012.

Physico chemical variables February May August November

C1 C2 C3 C1 C2 C3 C1 C2 C3 C1 C2 C3

T (◦ C) 29.19 29.16 29.65 29.41 28.81 28.88 28.64 28.54 28.56 27.78 28.39 28.23
pH 6.28 7.28 7.40 7.70 7.67 7.75 6.74 7.14 6.98 6.30 6.50 6.30
EC (␮S cm−1 ) 62.00 57.00 57.00 47.00 45.00 50.00 64.00 54.00 56.00 94.00 89.00 90.00
TDS (mg L−1 ) 31.00 28.00 29.00 23.00 22.50 25.00 32.00 27.00 28.00 47.00 45.00 45.00
SAL (mg L−1 ) 0.03 0.03 0.03 0.02 0.02 0.02 0.03 0.02 0.02 0.04 0.04 0.04
DO (mg L−1 ) 6.28 7.65 7.00 5.31 5.42 5.85 3.23 3.94 3.95 8.77 8.96 8.91
Transparency (cm) 40.00 70.00 45.00 60.00 70.00 70.00 80.00 70.00 100.00 70.00 60.00 60.00
TRB (UNT) 10.00 6.00 10.00 5.00 5.00 6.00 3.50 4.00 4.50 16.00 21.00 18.00
COLOR (UC) 16.00 20.00 19.00 24.00 24.00 32.00 25.20 28.00 34.50 22.00 15.00 25.00
TSS (mg L−1 ) 14.00 16.00 20.00 4.00 5.00 6.00 4.00 3.00 3.50 8.00 6.00 8.00
COD (mg L−1 ) 21.00 24.00 24.00 24.00 14.00 18.00 65.00 28.00 28.00 22.00 27.00 20.00
BOD (mg L−1 ) 12.00 19.00 12.00 13.00 8.00 8.00 20.00 16.00 14.00 18.00 16.00 16.00
N-NO2 − (mg L−1 ) 1.53 0.11 2.33 0.64 0.24 0.49 6.27 5.25 5.34 0.68 0.59 0.63
N-NO3 − (mg L−1 ) 0.04 0.01 0.01 0.02 0.02 0.02 0.03 0.01 0.03 0.26 0.19 0.13
N-NH4 (mg L−1 ) 1.01 0.03 0.13 1.17 0.17 0.22 0.29 0.16 0.22 0.76 0.43 8.93
P04 3− (mg L−1 ) 0.72 0.56 0.99 0.72 1.19 1.04 1.02 0.16 0.62 0.82 0.87 0.06
SO4 2− (mg L−1 ) 67.60 54.06 62.76 4.77 3.93 4.75 10.03 11.79 11.13 5.89 5.67 6.12
F− (mg L−1 ) 0.36 0.24 0.33 0.97 0.16 1.04 1.20 0.33 0.43 0.18 0.15 0.07
Hardness (mg L−1 ) 12.45 11.97 13.56 6.04 5.80 6.02 4.43 4.91 5.00 6.05 5.53 7.36
Alkalinity (mg L−1 ) 40.00 20.00 20.00 15.00 20.00 10.00 60.00 40.00 40.00 20.00 15.00 15.00
Cl− (mg L−1 ) 4.11 3.36 3.88 3.86 3.07 3.53 3.88 2.54 2.65 6.78 5.96 6.48
NH3 (mg L−1 ) 1.01 0.03 0.13 1.17 0.17 0.22 0.29 0.16 0.22 0.76 0.43 8.93
530 B.N.S. Costa et al. / Ecological Indicators 61 (2016) 526–545

Table 4
Seasonal variation of physicochemical variables in the Murucupi River in 2012.

Physico chemical variables February May August November

M1 M2 M3 M1 M2 M3 M1 M2 M3 M1 M2 M3

T (◦ C) 27.55 28.56 30.14 26.91 27.89 29.11 28.52 28.86 29.62 28.15 28.22 29.14
pH 6.06 6.36 6.80 7.61 7.46 7.05 6.87 6.20 6.35 6.03 6.25 6.69
EC (␮S cm−1 ) 61.00 70.00 55.00 69.00 68.00 45.00 67.00 61.00 41.00 209.00 215.00 252.00
TDS (mg L−1 ) 30.00 35.00 28.00 34.00 34.00 23.00 34.00 31.00 21.00 104.00 108.00 126.00
SAL (mg L−1 ) 0.03 0.03 0.02 0.03 0.02 0.02 0.03 0.03 0.02 0.10 0.40 0.12
DO (mg L−1 ) 2.04 2.52 5.56 2.26 4.95 6.35 4.85 3.83 5.47 3.32 3.54 5.58
Transparency (cm) 20.00 20.00 50.00 40.00 40.00 60.00 70.00 40.00 80.00 70.00 70.00 70.00
TRB (UNT) 58.00 48.00 32.00 19.00 18.00 18.00 22.00 28.00 22.00 13.00 12.00 10.00
COLOR (UC) 25.00 22.00 27.00 12.00 21.00 30.00 50.00 58.00 47.00 33.00 14.00 64.00
TSS (mg L−1 ) 30.00 22.00 26.00 13.00 13.00 9.00 9.00 17.00 12.00 4.00 2.00 3.00
COD (mg L−1 ) 32.00 12.00 20.00 34.00 42.00 33.00 20.00 29.00 10.00 12.00 17.00 16.00
BOD (mg L−1 ) 21.44 8.04 13.40 22.78 28.14 22.11 13.40 19.43 6.70 8.04 11.39 10.72
N-NO2 − (mg L−1 ) 6.57 15.77 6.79 3.11 2.82 1.00 2.17 1.20 1.21 0.61 0.65 0.56
N-NO3 − (mg L−1 ) 0.06 0.05 0.07 0.20 0.20 0.16 0.04 0.09 0.09 0.12 0.11 0.19
N-NH4 (mg L−1 ) 0.04 0.11 0.19 0.92 0.55 0.06 0.20 0.16 1.14 1.13 0.25 0.57
P-P04 3− (mg L−1 ) 0.53 0.62 0.67 0.02 0.03 0.05 0.21 0.03 0.07 0.17 0.15 0.11
SO4 2− (mg L−1 ) 3.92 7.18 7.36 2.79 2.42 1.48 1.53 1.19 1.43 7.46 8.00 1.46
F− (mg L−1 ) 0.03 0.07 0.05 0.04 0.04 0.03 0.02 0.02 0.02 0.03 0.03 0.02
Hardness (mg L−1 ) 8.59 11.85 11.65 3.85 4.48 5.37 4.54 4.59 3.74 8.09 8.38 3.32
Alkalinity (mg L−1 ) 5.00 10.00 10.00 20.00 30.00 30.00 20.00 40.00 35.00 10.00 10.00 12.00
Cl− (mg L−1 ) 11.25 9.93 6.36 9.40 7.55 3.24 4.60 2.86 2.69 42.43 45.45 42.89
NH3 (mg L−1 ) 0.03 0.09 0.16 0.75 0.45 0.05 0.17 0.13 0.94 0.93 0.20 0.47

2.6. Zooplankton January to April and then decreased, demonstrating a nearly con-
sistent behavior from June to December (Fig. 2A).
The qualitative analyses of the zooplankton community were However, the maximum temperature and relative humidity had
carried out via the sub-sampling of a 6 mL aliquot in Petri dishes, inversely proportional behaviors (Fig. 2B). The lowest temperatures
visualized under an inverted optical microscope (Axiovert 40C, Carl and highest relative humidity rates were recorded from January
Zeiss) coupled to an image capture system (AxiocamMRc). The tax- to April. From May onward, an inversion in this characteristic
onomic identification of the organisms was performed to the most was noted, and the regions that presented high temperatures also
specific possible level. showed a decrease in humidity. Despite these oscillations, the rel-
To determine the total density of the zooplankton commu- ative humidity was high throughout the year, ranging from 74% to
nity (org. m−3 ), quantitative analyses were performed using the 91%.
subsample sedimentation method and were observed through an Based on the WQI, we observed that the Arapiranga is the only
inverted optical microscope (Axiovert 40C, Carl Zeiss) with 200× river with a classification of “good” according to water analyses.
magnification (Utermöhl, 1958; Garzio and Steinberg, 2013). The Curuperê-Dendê and Murucupi rivers recorded “fair” water on
Depending on the degree of occurrence of zooplankton, average; however, at many points along Murucupi, the WQI cal-
they were classified as very frequent (Fr ≥ 70%), frequent culation classified waters as “marginal,” mainly at points closer to
(30% ≤ Fr > 70%), infrequent (10% ≤ Fr > 30%), or sporadic (Fr < 10%). domestic and sanitary effluent discharge areas (Table 1).
Data on the physico-chemical variables of water related to the
2.7. Statistics Arapiranga, Curuperê-Dendê, and Murucupi rivers are presented in
Tables 2, 3, and 4, respectively. The PCA (Fig. 3A), which was gen-
Multivariate analyses were applied to test the differences in the erated based on the physico-chemical parameters of water in the
limnological variables of surface waters among the sampling points Arapiranga, Curuperê-Dendê, and Murucupi rivers, revealed four
and seasonal periods. After organizing and standardizing the data, divergent groups (A, B, C, and D). The PC1 (20.3%) allowed for a
principal component analysis (PCA) was performed (Legendre and clear separation between groups C (quadrant III) and D (quadrant
Legendre, 2012) using the Minitab 17 program (Minitab Inc., USA). IV), while PC2 (15.7%) separated group A (quadrant I) from groups
In order to assess organism composition similarity and density C and D. The influences of the physico-chemical variables of the
levels among the points and periods of the rivers studied, a Non- groups can be observed in Fig. 3B.
Metric Multidimensional Scaling (NMDS) was used (Legendre and Group A of the PCA includes all data points of the Curuperê-
Legendre, 2012). To check for significant differences between the Dendê and Murucupi rivers in February. This cluster is related to
groups ordered by n-MDS, Bifactor Analysis of Similarity (ANOSIM) the increases in sulfate, nitrate, phosphate, pH, hardness, and tur-
was performed (Clarke and Warwick, 2011). These analyses were bidity (Fig. 3B). Group B is comprised of samples from A3 of the
completed using the R.Project program available at http://www.r- Arapiranga River from February, May, and August, the all 3 locations
project.org. (M1, M2, and M3) of the Murucupi River, from May and August, as
well as all the data points from the Curuperê-Dendê corresponding
3. Results to samples taken in May, August, and November (C1, C2, and C3).
Unlike the other groups, this one was not strongly influenced by
3.1. Limnology any single variable. Group C includes all samples from all points
in May and points 1 and 2 from February, August, and November
According to the total precipitation values and wind speed, in from the Arapiranga. In this group, the relationships are based on
2012, the monthly rainfall increased from January to March (higher increases in the variables Transparency, COD, BOD, lower pH, and
rainfall) (Fig. 2A). Soon after, rain gradually decreased, from April hardness. Group D is comprised of samples in November taken from
to October, with an increase in intensity increased again after the Murucupi River; the water of this river ranged in classifica-
November. The wind speed in the region increased gradually from tion from “fair” next to the sources (M1 and M2), to “good” next
B.N.S. Costa et al. / Ecological Indicators 61 (2016) 526–545 531

A 5
I A 2F II
3F River
4 1F3F Arapiranga
1F Curuperê-Dendê
3 Murucupi
2F

2
PC2 (15.9%) B
1A 2M
1 1M
3F 2M1M
3M
2A 2A 2N
3A 3M
0 1F 3A 1N
2F 3N 1A
C D
3A
3N
-1 2A
3M 1N
2N

2N
1N
-2 2M
1A
3N
1M
-3

III IV
-4
-4 -2 0 2 4 6 8
PC1 (20.5%)

B 0,5
HARDNESS

0,4
TSS
Nitrate-N
Sulfate
0,3 Phosphate
pH T
TRB
0,2
PC2 (15.9%)

BOD

0,1
Fluoride
COD
ALKALINITY
EC
0,0 Total Density TDS
Ammonia SAL
NitrogenAmonniacal Nitrite-N Chloride
-0,1 DO

-0,2 COLOR

Transparency
-0,3

-0,2 -0,1 0,0 0,1 0,2 0,3 0,4 0,5

PC1 (20.5%)

Fig. 3. PCA for physicochemical variables in the Arapiranga, Curuperê-Dendê and Murucpi Rivers in 2012. (A) Score plot for the first 2 components; (B) loading plot for the
first 2 components

to the river mouth (M3), Samples from November were distributed in all samples (100%) included Cyclopoida copepodites, Cope-
according to correlation with EC, TDS, SAL, and chlorides. poda nauplius, Codonella cratera, and Keratella cochlearis. In the
Curuperê-Dendê, the most frequent taxa (100%) were Cyclopoida
3.2. Zooplankton community copepodites, Copepoda nauplius, Codenella sp1, Tintinnina sp1,
Bdelloidea sp2, Keratella lenzi, Keratella cochlearis, and Keratella
The total of 149 taxa was detected in the three rivers, com- americana. In the Murucupi River, the groups with a frequency of
prising thirty-four genera, twenty-four families, eleven orders, 100% were Cyclopoida sp1, Cyclopoida copepodites, Copepod Nau-
ten classes, and seven phyla. The most representative fami- plius, Bosminopsis deitersi, Cladocera egg, Bdelloidea sp2, Keratella
lies were Difflugiidae (21 species), followed by Arcellidae (17 lenzi, Keratella cochlearis, and Filinia terminalis.
species), Brachionidae (15 species), Lecanidae (12 species), Tri- According to the similarity test, (ANOSIM), the composition and
chotriidae (10 species), and finally Euglyphidae and Trichocercidae density of the zooplankton community is significantly different
(both with 9 species). Tables 5–7 show the taxonomic compo- among the three rivers studied (r = 0.275; p = 0.001). Only the Arapi-
sition and classification of the species and groups recorded in ranga River (r = 0.506; p = 0.002) was different among the sampling
the Arapiranga, Curuperê-Dendê, and Murucupi rivers, respec- months.
tively. Spatially, the density of zooplankton organisms was vari-
According to the frequency of occurrence, the taxa were clas- able (Fig. 4); the Arapiranga River had the lowest mean
sified as very frequent (14%), frequent (32%), infrequent (50%), values (75,847 org. m−3 ), followed by the Curuperê-Dendê
or sporadic (66%). In the Arapiranga River, the taxa present (97,931 org. m−3 ) and Murucupi (190,597 org. m−3 ).
532 B.N.S. Costa et al. / Ecological Indicators 61 (2016) 526–545

Table 5
Classification and frequency of occurrence of zooplankton taxa in the Arapiranga River in 2012.

Taxa February May August November FR (%) Classification

A1 A2 A3 A1 A2 A3 A1 A2 A3 A1 A2 A3

Phylum: Rotifera
Class: Eurotatoria
Order: Flosculariaceae
Family: Hexarthridae
Genera: Hexarthra Schmarda, 1854
Hexarthra sp.
Hexarthra sp1
Family: Trochosphaeridae
Genera: Filinia Bory de St. Vincent,
1824
Filinia camasecla Myers, 1938 x x 17 Infrequent
Filinia longiseta Ehrenberg, 1834 x x x x x x x 58 Frequent
Filinia opoliensis Zacharias, 1898 x 8 Sporadic
Filinia terminalis Plate, 1886 x x x x x x x 58 Frequent
Order: Ploima
Family: Asplanchnidae
Genera: Asplanchna Gosse, 1850
Asplanchna sp1 x 8 Sporadic
Asplanchna sp2
Family: Brachionidae
Genera: Anuraeopsis Lauterborn,
1990
Anuraeopsis sp1
Anuraeopsis sp2
Anuraeopsis sp3 x x 17 Infrequent
Genera: Brachionus Pallas, 1766
Brachionus calyciflorus gigantea x 8 Sporadic
Koste & Shiel, 1987
Brachionus caudatus Barrois & x x x x x x 50 Frequent
Daday, 1984
Brachionus caudatus personatus x 8 Sporadic
Ahlstrom, 1940
Brachionus gessneri Hauer, 1956 x x x x 33 Frequent
Brachionus mirus Daday, 1905 x x x x x x 50 Frequent
Brachionus urceolaris Müller, 1773 x x x x x x x 58 Frequent
Brachionus zahniseri gessneri
Hauler, 1956
Genera: Keratella Bory de St.
Vincent, 1822
Keratella americana Carlin, 1943 x x x x x x x x x x 83 Very frequent
Keratella cochlearis Gosse, 1851 x x x x x x x x x x x x 100 Very frequent
Keratella lenzi Hauer, 1937 x x x x x x x x x 75 Very frequent
Keratella sp1
Genera: Platyias Harring, 1913
Platyias quadricornis Ehrenberg, x 8 Sporadic
1832
Family: Euchlanidae
Genera: Dipleuchlanis Beauchamp,
1910
Dipleuchlanis propatula Gosse, 1886 x 8 Sporadic
Family: Lecanidae
Genera: Lecane Nitzsch, 1827
Lecane curvicornis Murray, 1913
Lecane ludwigi Eckstein, 1883
Lecane proiectaHauer, 1956 x x x 25 Infrequent
Lecane pusilla Harring, 1914
Lecane sp1
Genera: Monostyla Ehrenberg, 1830
M onostyla cornuta Müller, 1786
Monostyla bulla Gosse, 1851
Monostyla decipiens Murray, 1913 x x 17 Infrequent
Monostyla elachis Harring & Myers, x x x x 33 Frequent
1926
Monostyla lunaris Ehrenberg, 1832
Monostyla scutata Harring & Myers, x 8 Sporadic
1926
Monostyla sp1 x 8 Sporadic
Family: Lepadellidae
Genera: Lepadella Bory de St.
Vincent, 1826
Lepadella rottenburgi Lucks 1912 x x 17 Infrequent
Lepadella sp. x 8 Sporadic
Lepadella sp1 x 8 Sporadic
Family: Mytilinidae
B.N.S. Costa et al. / Ecological Indicators 61 (2016) 526–545 533

Table 5 (Continued)

Taxa February May August November FR (%) Classification

A1 A2 A3 A1 A2 A3 A1 A2 A3 A1 A2 A3

Genera: Mytilina Bory de St.


Vincent, 1826
Mytilina macrocera Jennings, 1894
Family: Synchaetidae
Genera: Polyarthra Ehrenberg,
1834
Polyarthra sp1 x x 17 Infrequent
Polyarthra sp2
Genera: Synchaeta Ehrenberg, 1832
Synchaeta sp1
Synchaeta sp2
Synchaeta sp3
Family: Testudinellidae
Genera: Testudinella Bory de St.
Vincent, 1826
Testudinella patina Hermann, 1783
Family: Trichocercidae
Genera: Trichocerca Lamarck, 1801
Trichocerca bicristata Gosse, 1887 x 8 Sporadic
Trichocerca capucina Wierzejski & x 8 Sporadic
Zacharias, 1893
Trichocerca gracilis Tessin, 1890
Trichocerca jenningsi Voigt, 1957 x 8 Sporadic
Trichocerca pusilla Jennings, 1903 x 8 Sporadic
Trichocerca ruttneri Donner, 1953 x 8 Sporadic
Trichocerca similis grandis Hauer,
1965
Trichocerca similis Wierzejski, 1893 x x x x 33 Frequent
Trichocerca sp1
Family: Trichotriidae
Genera: Trichotria Bory de St.
Vincent, 1827
Trichotria tetractis Ehrenberg, 1830 x 8 Sporadic
Order: Bdelloidea
Bdelloidea sp2 x x x x x x x x x x 83 Very frequent
Bdelloidea sp3 x x x x x x x x x x 83 Very frequent
Bdelloidea sp4 x x 17 Infrequent
Bdelloidea sp5 x x x x x 42 Frequent
Bdelloidea sp7 x 8 Sporadic
Bdelloidea sp8 x x x 25 Infrequent
Bdelloidea sp 13 x x 17 Infrequent
Bdelloidea sp14 x x x x 33 Frequent
Bdelloidea sp15 x 8 Sporadic
Phylum: Lobosa
Class: Testacealobosa
Order: Arcellinida
Family: Arcellidae
Genera: Arcella Ehrenberg, 1832
Arcella braziliensis Cunha, 1913 x 8 Sporadic
Arcella costata angulosa Playfair,
1918
Arcella costata Ehrenberg, 1847 x x 17 Infrequent
Arcella crenulata Deflandre, 1928
Arcella discoides Ehrenberg, 1871 x x 17 Infrequent
Arcella gibbosa Pénard, 1890
Arcella hemisphaerica gibba
Deflandre, 1928
Arcella hemisphaerica x x x 25 Infrequent
hemisphaerica Perty, 1852
Arcella megastoma Pénard, 1913 x 8 Sporadic
Arcella rotundata alta Playfair, 1918
Arcella rotundata aplanata
Deflandre, 1928
Arcella sp. x 8 Sporadic
Arcella sp1
Arcella sp4
Arcella vulgaris Ehrenberg, 1830 x x x x x x 50 Frequent
Arcella vulgaris undulata Deflandre, x 8 Sporadic
1928
Arcella vulgaris wailesi Deflandre, x 8 Sporadic
1928
Family: Centropyxidae
Genera: Centropyxis Stein, 1857
Centropyxis aculeata Ehrenberg, x x x x x x x x x x 83 Very frequent
1838
534 B.N.S. Costa et al. / Ecological Indicators 61 (2016) 526–545

Table 5 (Continued)

Taxa February May August November FR (%) Classification

A1 A2 A3 A1 A2 A3 A1 A2 A3 A1 A2 A3

Centropyxis cassis Wallich, 1864 x x x x x x 50 Frequent


Centropyxis ecornis Ehrenberg, x 8 Sporadic
1841
Centropyxis sp1 x 8 Sporadic
Genera: Cyclopyxis Deflandre, 1929
Cyclopyxis kahli Deflandre, 1929 x x x 25 Infrequent
Family: Difflugiidae
Genera: Difflugia Leclerc, 1815
Difflugia achlora Pénard, 1902
Difflugia acuminata Ehrenberg,
1838
Difflugia brevicolla Cash &
Hopkinson, 1909
Difflugia cf. minuta Rampi, 1950
Difflugia corona Wallich, 1864
Difflugia cylindrus Odgen, 1983
Difflugia distenda Odgen, 1983 x x x x x x 50 Frequent
Difflugia elegans Penard, 1890 x x x x x x x x 67 Frequent
Difflugia kempnyi Stepánek, 1953 x 8 Sporadic
Difflugia litophila Pénard, 1902
Difflugia penardi Hopkinson, 1909 x 8 Sporadic
Difflugia pyriformes Perty, 1849 x 8 Sporadic
Difflugia sp. Leclerc, 1815 x x x x x x x x 67 Frequent
Difflugia sp1 x x x x x x 50 Frequent
Difflugia sp2
Difflugia sp3
Difflugia sp4 x 8 Sporadic
Difflugia sp7 x x x x 33 Frequent
Difflugia sp10
Difflugia sp11
Difflugia sp13
Family: Lesquereusiidae
Genera: Lesquereusia
Schlumberger,1845
Lesquereusia sp1 x x x 25 Infrequent
Lesquereusia sp12
Genera: Netzelia Odgen, 1979
Netzelia sp. x x 17 Infrequent
Netzelia wailesi Ogden, 1980 x x x x 33 Frequent
Phylum: Cercozoa
Class: Imbricatea
Order: Euglyphida
Family: Ccyphoderidae
Genera: Cyphoderia Schlumberger,
1845
Cyphoderia sp1
Family: Euglyphidae
Genera: Euglypha Dujardin, 1840
Euglypha acanthophora Ehrenberg, x x x 25 Infrequent
1841
Euglypha denticulata Brown, 1912 x x 17 Infrequent
Euglypha filifera Pénard, 1890
Euglypha sp1 x 8 Sporadic
Genera: Trinema Dujardin, 1838
Trinema sp1 x x 17 Infrequent
Phylum: Ciliophora
Class: Polihymenophorea
Order: Oligotrichida
Tintinnina sp1 x x x x x x x x x x x 92 Very frequent
Tintinnina sp3 x 8 Sporadic
Tintinnina sp6
Tintinnina sp11
Family: Codonellidae
Genera: Codonella Haeckel 1873
Codonella cratera Leidy, 1877 x x x x x x x x x x x x 100 Very frequent
Phylum: Arthropoda
Class: Branchiopoda
Order: Diplostraca
Neonato de cladocera x x x x x x x 58 Frequent
Ovo de cladocera x x x x x x x 58 Frequent
Family: Bosminidae
Genera: Bosmina Baird, 1845
Bosmina hagmanni Stingelin, 1904 x x x x x x 50 Frequent
Bosmina longirostris Müller, 1785 x x x x x x x 58 Frequent
B.N.S. Costa et al. / Ecological Indicators 61 (2016) 526–545 535

Table 5 (Continued)

Taxa February May August November FR (%) Classification

A1 A2 A3 A1 A2 A3 A1 A2 A3 A1 A2 A3

Bosmina sp.
Genera: Bosminopsis Richard, 1895
Bosminopsis deitersi Richard, 1895 x x x x x x x x x x x 92 Very frequent
Family: Chydoridae
Genera: Alonella Fryer 1968
Alonella dadayi Birge, 1910 x x 17 Infrequent
Family: Sididae
Genera: Diaphanosoma
Diaphanosoma birgei Korinek, 1981
Family: Daphniidae
Genera: Ceriodaphinia
Ceriodaphinia cornuata Sars, 1885 x x x 25 Infrequent
Family: Macrothricidae
Genera: Macrothrix Baird, 1843
Macrothrix sp1
Family: Moinidae
Genera: Moina
Moina minuta Hansen, 1899 x x x x x x 50 Frequent
Class: Maxillopoda
Nauplio de Copepoda x x x x x x x x x x x x 100 Very frequent
Order: Cyclopoida
Copepodito de Cyclopoida x x x x x x x x x x x x 100 Very frequent
Cyclopoida sp1 x x x x x x x x x x x 92 Very frequent
Cyclopoida sp2
Cyclopoida sp3
Cyclopoida sp4
Cyclopoida sp5
Order: Calanoida
Calanoida sp1 x x x x x x x x x 75 Very frequent
Copepodito de Calanoida x x x x x x x 58 Frequent
Order: Haparcticoida
Copepodito de Haparcticoida
Haparcticoida sp1 x x x 25 Infrequent
Haparcticoida sp2
Class: Malacostraca
Order: Isopoda
Isopoda
Phylum: Mollusca
Class: Gastropoda
Larva de Gastropoda x x x x x 42 Frequent
Class: Bivalvia
Larva de Bivalve x x x x x 42 Frequent
Phylum: Annelida
Class: Polychaeta
Poliqueta x 8 Sporadic

In the Arapiranga River, Thecamoeba were positively corre-


lated to COLOR (r = 0.666; p = 0.018), COD (r = 0.618; p = 0.032), BOD
(r = 0.698; p = 0.012), and inversely correlated to TRB (r = −0.785;
300000
p = 0.003) and hardness (r = −0.591; p = 0.043). In the Curuperê-
Dendê River, they were correlated only to fluoride (r = 0.777;
Total Density (org.m-3 )

250000
p = 0.003) and in the Murucupi, there was no correlation to any
200000 physico-chemical variables.
Rotifers were correlated to ammonium N (r = 0.863; p = 0.000)
150000
and ammonia (r = 0.857; p = 0.000) in Arapiranga River. In the
100000 Curuperê-Dendê, there were influences on density associated with
COD (r = 0.826; p = 0.001) and in the Murucupi, we observed a good
50000 correlation with SAL (r = 0.600; p = 0.039).
The Cladocera were correlated to COLOR (r = −0.817; p = 0.001)
0
in the Arapiranga and Curuperê-Dendê rivers, respectively.
May

May

May
November

November

November
February

February

February
August

August

August

3.3. Bioindicators
Arapiranga Curuperê-Dendê Murucupi

Samples The indicator species analysis (IndVal) revealed that the species
Keratella lenzi (t = 0.989; p = 0.005) and Anuraeopsis sp1 (r = 0.736;
Fig. 4. Total density of zooplankton organisms in the Arapiranga, Curuperê-Dendê p = 0.005) have a high fidelity and specificity to the Curuperê-
and Murucupi Rivers in 2012. Dendê and Murucupi rivers. The species Difflugia distenda (r = 0.663;
536 B.N.S. Costa et al. / Ecological Indicators 61 (2016) 526–545

Table 6
Classification and frequency of occurrence of zooplankton taxa in the Curuperê-Dendê River in 2012.

Taxa February May August November FR (%) Classification

C1 C2 C3 C1 C2 C3 C1 C2 C3 C1 C2 C3

Phylum: Rotifera
Class: Eurotatoria
Order: Flosculariaceae
Family: He1arthridae
Genera: He1arthra Schmarda, 1854
He1arthra sp.
He1arthra sp1
Family: Trochosphaeridae
Genera: Filinia Bory de St. Vincent,
1824
Filinia camasecla Myers, 1938 x 8 Sporadic
Filinia longiseta Ehrenberg, 1834 x x x x x 42 Frequent
Filinia opoliensis Zacharias, 1898 x x x 25 Infrequent
Filinia terminalis Plate, 1886 x x x x x x x x x x x 92 Very frequent
Order: Ploima
Family: Asplanchnidae
Genera: Asplanchna Gosse, 1850
Asplanchna sp1 x x x 25 Infrequent
Asplanchna sp2
Family: Brachionidae
Genera: Anuraeopsis Lauterborn,
1990
Anuraeopsis sp1 x x x x x 42 Frequent
Anuraeopsis sp2 x 8 Sporadic
Anuraeopsis sp3
Genera: Brachionus Pallas, 1766
Brachionus calyciflorus gigantea
Koste & Shiel, 1987
Brachionus caudatus Barrois & x x x x x x 50 Frequent
Daday, 1984
Brachionus caudatus personatus x x x x x x 50 Frequent
Ahlstrom, 1940
Brachionus gessneri Hauer, 1956 x 8 Sporadic
Brachionus mirus Daday, 1905 x x x x x x x x x 75 Very frequent
Brachionus urceolaris Müller, 1773 x x x x x x x x x x 83 Very frequent
Brachionus zahniseri gessneri
Hauler, 1956
Genera: Keratella Bory de St.
Vincent, 1822
Keratella americana Carlin, 1943 x x x x x x x x x x x x 100 Very frequent
Keratella cochlearis Gosse, 1851 x x x x x x x x x x x x 100 Very frequent
Keratella lenzi Hauer, 1937 x x x x x x x x x x x x 100 Very frequent
Keratella sp1
Genera: Platyias Harring, 1913
Platyias quadricornis Ehrenberg,
1832
Family: Euchlanidae
Genera: Dipleuchlanis Beauchamp,
1910
Dipleuchlanis propatula Gosse, 1886
Family: Lecanidae
Genera: Lecane Nitzsch, 1827
Lecane curvicornis Murray, 1913 x x 17 Infrequent
Lecane ludwigi Eckstein, 1883
Lecane proiectaHauer, 1956 x x x x x 42 Frequent
Lecane pusilla Harring, 1914 x x x 25 Infrequent
Lecane sp1 x 8 Sporadic
Genera: Monostyla Ehrenberg, 1830
M onostyla cornuta Müller, 1786 x 8 Sporadic
Monostyla bulla Gosse, 1851 x x 17 Infrequent
Monostyla decipiens Murray, 1913 x x 17 Infrequent
Monostyla elachis Harring & Myers, x x 17 Infrequent
1926
Monostyla lunaris Ehrenberg, 1832 x 8 Sporadic
Monostyla scutata Harring & Myers,
1926
Monostyla sp1
Family: Lepadellidae
Genera: Lepadella Bory de St.
Vincent, 1826
Lepadella rottenburgi Lucks 1912 x x x 25 Infrequent
Lepadella sp.
Lepadella sp1 x 8 Sporadic
Family: Mytilinidae
B.N.S. Costa et al. / Ecological Indicators 61 (2016) 526–545 537

Table 6 (Continued)

Taxa February May August November FR (%) Classification

C1 C2 C3 C1 C2 C3 C1 C2 C3 C1 C2 C3

Genera: Mytilina Bory de St.


Vincent, 1826
Mytilina macrocera Jennings, 1894
Family: Synchaetidae
Genera: Polyarthra Ehrenberg,
1834
Polyarthra sp1 x 8 Sporadic
Polyarthra sp2 x 8 Sporadic
Genera: Synchaeta Ehrenberg, 1832
Synchaeta sp1
Synchaeta sp2 x x x x 33 Frequent
Synchaeta sp3 x x 17 Infrequent
Family: Testudinellidae
Genera: Testudinella Bory de St.
Vincent, 1826
Testudinella patina Hermann, 1783 x 8 Sporadic
Family: Trichocercidae
Genera: Trichocerca Lamarck, 1801
Trichocerca bicristata Gosse, 1887 x x x x x 42 Frequent
Trichocerca capucina Wierzejski & x 8 Sporadic
Zacharias, 1893
Trichocerca gracilis Tessin, 1890 x x x 25 Infrequent
Trichocerca jenningsi Voigt, 1957 x x x x x x 50 Frequent
Trichocerca pusilla Jennings, 1903
Trichocerca ruttneri Donner, 1953
Trichocerca similis grandis Hauer, x x x 25 Infrequent
1965
Trichocerca similis Wierzejski, 1893 x x x x x x 50 Frequent
Trichocerca sp1 x 8 Sporadic
Family: Trichotriidae
Genera: Trichotria Bory de St.
Vincent, 1827
Trichotria tetractis Ehrenberg, 1830
Order: Bdelloidea
Bdelloidea sp2 x x x x x x x x x x x x 100 Very frequent
Bdelloidea sp3 x x x x x x x x 67 Frequent
Bdelloidea sp4
Bdelloidea sp5 x x x x x x x x x 75 Very frequent
Bdelloidea sp7
Bdelloidea sp8 x x x x x x x 58 Frequent
Bdelloidea sp 13 x 8
Bdelloidea sp14 x x x 25 Infrequent
Bdelloidea sp15 x x x 25 Infrequent
Phylum: Lobosa
Class: Testacealobosa
Order: Arcellinida
Family: Arcellidae
Genera: Arcella Ehrenberg, 1832
Arcella braziliensis Cunha, 1913
Arcella costata angulosa Playfair, x x x 25 Infrequent
1918
Arcella costata Ehrenberg, 1847 x x 17 Infrequent
Arcella crenulata Deflandre, 1928
Arcella discoides Ehrenberg, 1871 x x x x x 42 Frequent
Arcella gibbosa Pénard, 1890 x 8
Arcella hemisphaerica gibba x 8
Deflandre, 1928
Arcella hemisphaerica x x x x x x x x 67 Frequent
hemisphaerica Perty, 1852
Arcella megastoma Pénard, 1913 x 8
Arcella rotundata alta Playfair, 1918 x 8
Arcella rotundata aplanata x x x 25 Infrequent
Deflandre, 1928
Arcella sp. x x x x 33 Frequent
Arcella sp1
Arcella sp4 x 8
Arcella vulgaris Ehrenberg, 1830 x x x x x x x x 67 Frequent
Arcella vulgaris undulata Deflandre, x x x x 33 Frequent
1928
Arcella vulgaris wailesi Deflandre, x x 17 Infrequent
1928
Family: Centropy1idae
Genera: Centropy1is Stein, 1857
Centropy1is aculeata Ehrenberg, x x x x x x 50 Frequent
1838
538 B.N.S. Costa et al. / Ecological Indicators 61 (2016) 526–545

Table 6 (Continued)

Taxa February May August November FR (%) Classification

C1 C2 C3 C1 C2 C3 C1 C2 C3 C1 C2 C3

Centropy1is cassis Wallich, 1864 x x x x x 42 Frequent


Centropy1is ecornis Ehrenberg, x x x x x x 50 Frequent
1841
Centropy1is sp1
Genera: Cyclopy1is Deflandre, 1929
Cyclopy1is kahli Deflandre, 1929 x x x 25 Infrequent
Family: Difflugiidae
Genera: Difflugia Leclerc, 1815
Difflugia achlora Pénard, 1902 x 8 Sporadic
Difflugia acuminata Ehrenberg, x x 17 Infrequent
1838
Difflugia brevicolla Cash &
Hopkinson, 1909
Difflugia cf. minuta Rampi, 1950 x x x 25 Infrequent
Difflugia corona Wallich, 1864 x x x 25 Infrequent
Difflugia cylindrus Odgen, 1983 x 8 Sporadic
Difflugia distenda Odgen, 1983 x 8 Sporadic
Difflugia elegans Penard, 1890 x x x x 33 Frequent
Difflugia kempnyi Stepánek, 1953 x 8 Sporadic
Difflugia litophila Pénard, 1902
Difflugia penardi Hopkinson, 1909 x x 17 Infrequent
Difflugia pyriformes Perty, 1849
Difflugia sp. Leclerc, 1815 x x x x x 42 Frequent
Difflugia sp1 x x 17 Infrequent
Difflugia sp2 x x 17 Infrequent
Difflugia sp3
Difflugia sp4
Difflugia sp7
Difflugia sp10 x 8 Sporadic
Difflugia sp11 x x 17 Infrequent
Difflugia sp13 x x 17 Infrequent
Family: Lesquereusiidae
Genera: Lesquereusia
Schlumberger,1845
Lesquereusia sp1 x x x 25 Infrequent
Lesquereusia sp12 x 8 Sporadic
Genera: Netzelia Odgen, 1979
Netzelia sp.
Netzelia wailesi Ogden, 1980 x x 17 Infrequent
Phylum: Cercozoa
Class: Imbricatea
Order: Euglyphida
Family: Ccyphoderidae
Genera: Cyphoderia Schlumberger,
1845
Cyphoderia sp1
Family: Euglyphidae
Genera: Euglypha Dujardin, 1840
Euglypha acanthophora Ehrenberg, x 8 Sporadic
1841
Euglypha denticulata Brown, 1912 x x 17 Infrequent
Euglypha filifera Pénard, 1890 x 8 Sporadic
Euglypha sp1
Genera: Trinema Dujardin, 1838
Trinema sp1 x x 17 Infrequent
Phylum: Ciliophora
Class: Polihymenophorea
Order: Oligotrichida
Tintinnina sp1 x x x x x x x x x x x x 100 Very frequent
Tintinnina sp3 x x 17 Infrequent
Tintinnina sp6 x 8 Sporadic
Tintinnina sp11
Family: Codonellidae
Genera: Codonella Haeckel 1873
Codonella cratera Leidy, 1877 x x x x x x x x x x x x 100 Very frequent
Phylum: Arthropoda
Class: Branchiopoda
Order: Diplostraca
Neonato de cladocera x x x x x x x 58 Frequent
Ovo de cladocera x x x x x x x x x 75 Very frequent
Family: Bosminidae
Genera: Bosmina Baird, 1845
Bosmina hagmanni Stingelin, 1904 x x x x x 42 Frequent
Bosmina longirostris Müller, 1785 x x x x 33 Frequent
Bosmina sp.
B.N.S. Costa et al. / Ecological Indicators 61 (2016) 526–545 539

Table 6 (Continued)

Taxa February May August November FR (%) Classification

C1 C2 C3 C1 C2 C3 C1 C2 C3 C1 C2 C3

Genera: Bosminopsis Richard, 1895


Bosminopsis deitersi Richard, 1895 x x x x x x x x x x x 92 Very frequent
Family: Chydoridae
Genera: Alonella Fryer 1968
Alonella dadayi Birge, 1910 x 8 Sporadic
Family: Sididae
Genera: Diaphanosoma
Diaphanosoma birgei Korinek, 1981 x x x 25 Infrequent
Family: Daphniidae
Genera: Ceriodaphinia
Ceriodaphinia cornuata Sars, 1885
Family: Macrothricidae
Genera: Macrothri1 Baird, 1843
Macrothri1 sp1
Family: Moinidae
Genera: Moina
Moina minuta Hansen, 1899 x x x x x x x x 67 Frequent
Class: Ma1illopoda
Nauplio de Copepoda x x x x x x x x x x x x 100 Very frequent
Order: Cyclopoida
Copepodito de Cyclopoida x x x x x x x x x x x x 100 Very frequent
Cyclopoida sp1 x x x x x x x x x 75 Very frequent
Cyclopoida sp2 x x x x x 42 Frequent
Cyclopoida sp3 x x x 25 Infrequent
Cyclopoida sp4
Cyclopoida sp5
Order: Calanoida
Calanoida sp1 x 8 Sporadic
Copepodito de Calanoida x x x x x x x x 67 Frequent
Order: Haparcticoida
Copepodito de Haparcticoida
Haparcticoida sp1 x x 17 Infrequent
Haparcticoida sp2 x x 17 Infrequent
Class: Malacostraca
Order: Isopoda
Isopoda x 8 Sporadic
Phylum: Mollusca
Class: Gastropoda
Larva de Gastropoda x x x x x x x x x x 83 Very frequent
Class: Bivalvia
Larva de Bivalve x x x x x 42 Frequent
Phylum: Annelida
Class: Polychaeta
Poliqueta x x x x 33 Frequent

p = 0.015) and Difflugia sp7 (r = 0.577; p = 0.010) were most abun- intense human occupation on river banks with poorly managed
dant in the Arapiranga River. sanitary conditions, and the use of the river bed for recreational
activities (Carvalho et al., 2000). In February, the WQI of the Muru-
4. Discussion cupi River varied from marginal (M1) to fair (M2 and M3), while
it was consistently fair for the Curuperê-Dendê River; confirming
4.1. Limnology water degradation has occurred in these environments, possibly
due to the above-mentioned factors.
There have been few systematic studies that consider winds to Group B, consists of more data points, most of which are from
be direct or indirect factors influencing zooplankton distribution, samples obtained in the less rainy months. The absence of char-
and most dismiss the possibility that they could rapidly alter the acteristic physico-chemical variables associated with this group
limnological characteristics of aquatic ecosystems (Pinheiro et al., might be due to the influence of the Pará River, since the title regime
2013). from this river is the main source during the rainy period (Gregório
Zooplankton is sensitive to temperature changes since their and Mendes, 2009). The distribution of data points in group C is
metabolism is directly affected by abrupt shifts in this environmen- linked with increases in transparency, COD, and BOD, which might
tal parameter (Benndorf et al., 2001; Smith et al., 2012). However, be due to decomposition of (humic) vegetables. The overall dis-
temperature is not a determining factor for the zooplankton com- tribution of all data points is also linked to the characteristics of
munity in tropical regions where variations are relatively negligible this river, with a long extension and greater distance between its
throughout the year (Magalhães et al., 2011). sources and mouth at the Pará River. Closer to the sources of the
In group A of the PCA, the increase in sulfate, nitrate, phosphate, river, the riparian forests are more preserved, which decreases the
pH, hardness, and turbidity coincides with the rainiest period in pH, due to the high concentration of humic substances (Yin et al.,
the region. This might be explained by rainwater leaching nutrients 2011).
from the terrestrial to aquatic ecosystems. The differences observed In group D, November was correlated to EC, TDS, SAL, and chlo-
among these rivers might be associated to some specific character- ride concentration. In this month, there was less rain; therefore,
istics, including: the close proximity of devastated riparian forests, the main influence during this period might be associated with
540 B.N.S. Costa et al. / Ecological Indicators 61 (2016) 526–545

Table 7
Classification and frequency of occurrence of taxa organisms in the Murucupi River in 2012.

Taxa February May August November FR (%) Classification

M1 M2 M3 M1 M2 M3 M1 M2 M3 M1 M2 M3

Phylum: Rotifera
Class: Eurotatoria
Order: Flosculariaceae
Family: He1arthridae
Genera: He1arthra Schmarda, 1854
He1arthra sp.
He1arthra sp1 x x 17 Infrequent
Family: Trochosphaeridae
Genera: Filinia Bory de St. Vincent,
1824
Filinia camasecla Myers, 1938 x x x 25 Infrequent
Filinia longiseta Ehrenberg, 1834 x x x x x 42 Frequent
Filinia opoliensis Zacharias, 1898 x x x 25 Infrequent
Filinia terminalis Plate, 1886 x x x x x x x x x x x x 100 Very frequent
Order: Ploima
Family: Asplanchnidae
Genera: Asplanchna Gosse, 1850
Asplanchna sp1 x x 17 Infrequent
Asplanchna sp2 x 8 Sporadic
Family: Brachionidae
Genera: Anuraeopsis Lauterborn,
1990
Anuraeopsis sp1 x x x x x x x x 67 Frequent
Anuraeopsis sp2
Anuraeopsis sp3 x 8 Sporadic
Genera: Brachionus Pallas, 1766
Brachionus calyciflorus gigantea
Koste & Shiel, 1987
Brachionus caudatus Barrois & x x x x x x x x x 75 Very frequent
Daday, 1984
Brachionus caudatus personatus x x x x x 42 Frequent
Ahlstrom, 1940
Brachionus gessneri Hauer, 1956 x x x x 33 Frequent
Brachionus mirus Daday, 1905 x x x x x x x x x 75 Very frequent
Brachionus urceolaris Müller, 1773 x x x x x x x 58 Frequent
Brachionus zahniseri gessneri x x x x x x 50 Frequent
Hauler, 1956
Genera: Keratella Bory de St.
Vincent, 1822
Keratella americana Carlin, 1943 x x x x x x x x x x 83 Very frequent
Keratella cochlearis Gosse, 1851 x x x x x x x x x x x x 100 Very frequent
Keratella lenzi Hauer, 1937 x x x x x x x x x x x x 100 Very frequent
Keratella sp1 x 8 Sporadic
Genera: Platyias Harring, 1913
Platyias quadricornis Ehrenberg, x x 17 Infrequent
1832
Family: Euchlanidae
Genera: Dipleuchlanis Beauchamp,
1910
Dipleuchlanis propatula Gosse, 1886
Family: Lecanidae
Genera: Lecane Nitzsch, 1827
Lecane curvicornis Murray, 1913 x x 17 Infrequent
Lecane ludwigi Eckstein, 1883 x 8 Sporadic
Lecane proiectaHauer, 1956 x x x 25 Infrequent
Lecane pusilla Harring, 1914 x 8 Sporadic
Lecane sp1 x x x x 33 Frequent
Genera: Monostyla Ehrenberg, 1830
M onostyla cornuta Müller, 1786 x 8 Sporadic
Monostyla bulla Gosse, 1851 x x x x x x 50 Frequent
Monostyla decipiens Murray, 1913 x x x 25 Infrequent
Monostyla elachis Harring & Myers,
1926
Monostyla lunaris Ehrenberg, 1832
Monostyla scutata Harring & Myers,
1926
Monostyla sp1
Family: Lepadellidae
Genera: Lepadella Bory de St.
Vincent, 1826
Lepadella rottenburgi Lucks 1912 x 8 Sporadic
Lepadella sp. x x 17 Infrequent
Lepadella sp1 x 8 Sporadic
Family: Mytilinidae
B.N.S. Costa et al. / Ecological Indicators 61 (2016) 526–545 541

Table 7 (Continued)

Taxa February May August November FR (%) Classification

M1 M2 M3 M1 M2 M3 M1 M2 M3 M1 M2 M3

Genera: Mytilina Bory de St.


Vincent, 1826
Mytilina macrocera Jennings, 1894 x 8 Sporadic
Family: Synchaetidae
Genera: Polyarthra Ehrenberg,
1834
Polyarthra sp1 x x x x x x 50 Frequent
Polyarthra sp2
Genera: Synchaeta Ehrenberg, 1832
Synchaeta sp1 x x x 25 Infrequent
Synchaeta sp2 x x x x 33 Frequent
Synchaeta sp3
Family: Testudinellidae
Genera: Testudinella Bory de St.
Vincent, 1826
Testudinella patina Hermann, 1783 x x x x x 42 Frequent
Family: Trichocercidae
Genera: Trichocerca Lamarck, 1801
Trichocerca bicristata Gosse, 1887 x x x x x 42 Frequent
Trichocerca capucina Wierzejski & x x x x x 42 Frequent
Zacharias, 1893
Trichocerca gracilis Tessin, 1890
Trichocerca jenningsi Voigt, 1957 x x 17 Infrequent
Trichocerca pusilla Jennings, 1903
Trichocerca ruttneri Donner, 1953
Trichocerca similis grandis Hauer, x x x 25 Infrequent
1965
Trichocerca similis Wierzejski, 1893 x x x x x x 50 Frequent
Trichocerca sp1 x x x 25 Infrequent
Family: Trichotriidae
Genera: Trichotria Bory de St.
Vincent, 1827
Trichotria tetractis Ehrenberg, 1830 x 8 Sporadic
Order: Bdelloidea
Bdelloidea sp2 x x x x x x x x x x x x 100 Very frequent
Bdelloidea sp3 x x x x x x x x x 75 Very frequent
Bdelloidea sp4 x x x 25 Infrequent
Bdelloidea sp5 x x x x x x 50 Frequent
Bdelloidea sp7 x x x x 33 Frequent
Bdelloidea sp8 x x x x x x 50 Frequent
Bdelloidea sp 13 x x x x x 42 Frequent
Bdelloidea sp14 x x 17 Infrequent
Bdelloidea sp15 x x x x x x x x 67 Frequent
Phylum: Lobosa
Class: Testacealobosa
Order: Arcellinida
Family: Arcellidae
Genera: Arcella Ehrenberg, 1832
Arcella braziliensis Cunha, 1913
Arcella costata angulosa Playfair,
1918
Arcella costata Ehrenberg, 1847 x 8 Sporadic
Arcella crenulata Deflandre, 1928 x 8 Sporadic
Arcella discoides Ehrenberg, 1871 x x x 25 Infrequent
Arcella gibbosa Pénard, 1890
Arcella hemisphaerica gibba x x x 25 Infrequent
Deflandre, 1928
Arcella hemisphaerica x x x 25 Infrequent
hemisphaerica Perty, 1852
Arcella megastoma Pénard, 1913 x 8 Sporadic
Arcella rotundata alta Playfair, 1918 x x 17 Infrequent
Arcella rotundata aplanata
Deflandre, 1928
Arcella sp. x x x x x x x 58 Frequent
Arcella sp1 x 8 Sporadic
Arcella sp4
Arcella vulgaris Ehrenberg, 1830 x x x x x x x 58 Frequent
Arcella vulgaris undulata Deflandre, x 8 Sporadic
1928
Arcella vulgaris wailesi Deflandre,
1928
Family: Centropy1idae
Genera: Centropy1is Stein, 1857
Centropy1is aculeata Ehrenberg, x x x x x x x x x 75 Very frequent
1838
542 B.N.S. Costa et al. / Ecological Indicators 61 (2016) 526–545

Table 7 (Continued)

Taxa February May August November FR (%) Classification

M1 M2 M3 M1 M2 M3 M1 M2 M3 M1 M2 M3

Centropy1is cassis Wallich, 1864 x x x x x 42 Frequent


Centropy1is ecornis Ehrenberg, x 8 Sporadic
1841
Centropy1is sp1 x x 17 Infrequent
Genera: Cyclopy1is Deflandre, 1929
Cyclopy1is kahli Deflandre, 1929
Family: Difflugiidae
Genera: Difflugia Leclerc, 1815
Difflugia achlora Pénard, 1902
Difflugia acuminata Ehrenberg, x 8 Sporadic
1838
Difflugia brevicolla Cash & x 8 Sporadic
Hopkinson, 1909
Difflugia cf. minuta Rampi, 1950
Difflugia corona Wallich, 1864
Difflugia cylindrus Odgen, 1983 x x x 25 Infrequent
Difflugia distenda Odgen, 1983 x x 17 Infrequent
Difflugia elegans Penard, 1890 x x x 25 Infrequent
Difflugia kempnyi Stepánek, 1953 x 8 Sporadic
Difflugia litophila Pénard, 1902 x 8 Sporadic
Difflugia penardi Hopkinson, 1909 x 8 Sporadic
Difflugia pyriformes Perty, 1849
Difflugia sp. Leclerc, 1815 x x x x x 42 Frequent
Difflugia sp1 x x 17 Infrequent
Difflugia sp2
Difflugia sp3 x x 17 Infrequent
Difflugia sp4
Difflugia sp7
Difflugia sp10
Difflugia sp11
Difflugia sp13
Family: Lesquereusiidae
Genera: Lesquereusia
Schlumberger,1845
Lesquereusia sp1
Lesquereusia sp12
Genera: Netzelia Odgen, 1979
Netzelia sp.
Netzelia wailesi Ogden, 1980
Phylum: Cercozoa
Class: Imbricatea
Order: Euglyphida
Family: Ccyphoderidae
Genera: Cyphoderia Schlumberger,
1845
Cyphoderia sp1 x x 17 Infrequent
Family: Euglyphidae
Genera: Euglypha Dujardin, 1840
Euglypha acanthophora Ehrenberg, x x x x 33 Frequent
1841
Euglypha denticulata Brown, 1912 x 8 Sporadic
Euglypha filifera Pénard, 1890 x 8 Sporadic
Euglypha sp1
Genera: Trinema Dujardin, 1838
Trinema sp1
Phylum: Ciliophora
Class: Polihymenophorea
Order: Oligotrichida
Tintinnina sp1 x x x x x x x x x x x 92 Very frequent
Tintinnina sp3 x x 17 Infrequent
Tintinnina sp6 x 8 Sporadic
Tintinnina sp11 x x x x 33 Frequent
Family: Codonellidae
Genera: Codonella Haeckel 1873
Codonella cratera Leidy, 1877 x x x x x x x x x x 83 Very frequent
Phylum: Arthropoda
Class: Branchiopoda
Order: Diplostraca
Neonato de cladocera x x x x x x x x x x 83 Very frequent
Ovo de cladocera x x x x x x x x x x x x 100 Very frequent
Family: Bosminidae
Genera: Bosmina Baird, 1845
Bosmina hagmanni Stingelin, 1904 x x x x x x x x x x 83 Very frequent
Bosmina longirostris Müller, 1785 x x x x x x x x x x 83 Very frequent
B.N.S. Costa et al. / Ecological Indicators 61 (2016) 526–545 543

Table 7 (Continued)

Taxa February May August November FR (%) Classification

M1 M2 M3 M1 M2 M3 M1 M2 M3 M1 M2 M3

Bosmina sp. x x 17 Infrequent


Genera: Bosminopsis Richard, 1895
Bosminopsis deitersi Richard, 1895 x x x x x x x x x x x x 100 Very frequent
Family: Chydoridae
Genera: Alonella Fryer 1968
Alonella dadayi Birge, 1910 x x x x x 42 Frequent
Family: Sididae
Genera: Diaphanosoma
Diaphanosoma birgei Korinek, 1981
Family: Daphniidae
Genera: Ceriodaphinia
Ceriodaphinia cornuata Sars, 1885 x x x x x x x x 67 Frequent
Family: Macrothricidae
Genera: Macrothri1 Baird, 1843
Macrothri1 sp1 x 8 Sporadic
Family: Moinidae
Genera: Moina
Moina minuta Hansen, 1899 x x x x x x x x x 75 Very frequent
Class: Ma1illopoda
Nauplio de Copepoda x x x x x x x x x x x x 100 Very frequent
Order: Cyclopoida
Copepodito de Cyclopoida x x x x x x x x x x x x 100 Very frequent
Cyclopoida sp1 x x x x x x x x x x x x 100 Very frequent
Cyclopoida sp2 x x x x x x x 58 Frequent
Cyclopoida sp3 x x x 25 Infrequent
Cyclopoida sp4 x 8 Sporadic
Cyclopoida sp5 x x 17 Infrequent
Order: Calanoida
Calanoida sp1 x x 17 Infrequent
Copepodito de Calanoida x x x x x x 50 Frequent
Order: Haparcticoida
Copepodito de Haparcticoida x x 17 Infrequent
Haparcticoida sp1 x 8 Sporadic
Haparcticoida sp2 x x x x x x x 58 Frequent
Class: Malacostraca
Order: Isopoda
Isopoda
Phylum: Mollusca
Class: Gastropoda
Larva de Gastropoda x x x x x x x 58 Frequent
Class: Bivalvia
Larva de Bivalve x x x x x x 50 Frequent
Phylum: Annelida
Class: Polychaeta
Poliqueta x x x x 33 Frequent

anthropogenic factors, mainly input from domestic and sanitary Park and Marshall (2000) also observed growth in zooplank-
sewages, located near the sources of the river. These effluents ton biomass as the number of trophic levels in the environment
have many metallic, cationic, and anionic ions, which explain the increase, which also was found in this study, where the highest
increase in these variables during this period (Oboh et al., 2009). organism densities were recorded in the Murucupi River.
We observed that density values of the Thecamoeba were char-
acterized by slight seasonal variations and were present in different
4.2. Zooplankton community densities in the drainages studied. The highest densities in this
group were recorded in Arapiranga River, which was affected by
According to Navarro and Modenutti (2012), the differentiation less anthropogenic activities than the other rivers.
among the rivers, as assessed with the ANOSIM method, demon- The predominant presence of this group in the Arapiranga River
strates the unique characteristics of each environment, suggesting is explained, according to Madoni (1994), by the preference of
that anthropic activities change the biota in aquatic ecosystems. Thecamoeba for low organic rate environments. Silva (2011) also
The Arapiranga River was the only one that with seasonal dif- observed the better development of these organisms in environ-
ferences observed in the zooplankton community structure and ments with a lower anthropic impact.
the only one that received a water quality classification of “good” Rotifers were clearly influenced by geographical location and,
due to the limited anthropic impact along its margins. This allows therefore, showed distinct patterns among the three drainages. As
for natural factors of the region, such as rainfall, to exercise influ- was apparent in the studies of May and O’Hare (2005) and Wen et al.
ence over the ecosystem dynamics, leading to changes in the (2010), the lowest density of rotifers was found in the Arapiranga
abiotic and biotic environments (Navarro and Modenutti, 2012). River, suggesting that the discharge of domestic sewage provides
The Curuperê-Dendê and Murucupi rivers could not be differenti- an suitable environment for increased growth of these organisms.
ated seasonally; which emphasizes that the continuous discharge The highest densities of Cladocera were recorded in the Muru-
of domestic sewage in these rivers affects the natural Amazon cupi River and is mainly attributed to the species Bosminopsis
ecosystems, causing the zooplankton community to remain static deitersi, which dominates in oligotrophic environments (Heerkloss
throughout the year. and Schnese, 1999). However, their high density in the Murucupi,
544 B.N.S. Costa et al. / Ecological Indicators 61 (2016) 526–545

compared to the other rivers, is explained by their feeding char- biomanipulated Bautzen Reservoir (Germany). Freshw. Biol. 46, 199–211, http://
dx.doi.org/10.1046/j. 1365-2427.2000.00657.x.
acteristics. Cladocerans filter feed and is able to harvest nutrients
Carneiro, S.B., Vale, E.R., Lima, M.d.O., 2007. Atividades industriais no município de
more easily environments that have experienced eutrophication, Barcarena, Pará: Os impactos ambientais nos igarapés Curuperê e Dendê a partir
habitats which result in higher proliferation rates and persistent do lançamento de efluentes ácidos doprocesso de beneficiamento do caulim e
presence in these locations (Panosso et al., 2003). avaliação das águas de consumo das comunidades do Bairro Indus. Relatório
Técnico. Instituto Evandro Chagas, Belém.
Similar to the Rotifera and Cladocera, copepods demonstrated Carvalho, A.R., Schlittler, F.H., Tornisielo, V.L., 2000. Relações da atividade
the same pattern of density in the Murucupi River, and the com- agropecuária com parâmetros físicos químicos da água. Quim. Nova 23,
position of this group was mainly represented by the Cyclopoida 618–622.
Clark, G., 2005. The condition of the working class in England, 1209–2004. J. Polit.
nauplii and copepodites stages; these organisms also easily adapt Econ. 113, 1307–1340, http://dx.doi.org/10.1086/498123.
to eutrophic environments (Perbiche-Neves et al., 2013). Clarke, K.R., Warwick, R.M., 2011. Change in marine communities: an approach to
statistical analysis and interpretation, 2nd ed. PRIMER-E, Plymouth.
Davies, O.A., 2009. Spatio-temporal distribution, abundance and species composi-
4.3. Bioindicators tion of zooplankton of Woji-okpoka Creek, Port Harcourt, Nigeria. Res. J. Appl.
Sci. Eng. Technol. 1, 14–34.
Dussart, B.H., 1964. Les differentes categories de plancton., pp. 72–74.
The dominance of the genera Anuraeopsis and Keratella in the Eschenhagen, M., Schuppler, M., Röske, I., 2003. Molecular characterization of
Curuperê-Dendê and Murucupi rivers, which receive large amounts the microbial community structure in two activated sludge systems for the
of domestic sewage discharge, corroborates the work of Haberman advanced treatment of domestic effluents. Water Res. 37, 3224–3232, http://
dx.doi.org/10.1016/S0043-1354(03)00136-2.
and Haldna (2014), who demonstrated that species of these genera Etilé, R.N., Kouassi, A.M., Aka, M.N., Pagano, M., N’douba, V., Kouassi, N.J., 2008.
are indicative of environmental eutrophication. Spatio-temporal variations of the zooplankton abundance and composition in a
The species Difflugia distenda were most abundant in the Arapi- West African tropical coastal lagoon (Grand-Lahou, Côte d’Ivoire). Hydrobiologia
624, 171–189, http://dx.doi.org/10.1007/s10750-008-9691-7.
ranga River. In this study as well as that of Souza (2014), this species Faial, K.d.C.F., 2009. Avaliação Físico-Química e determinação de metais de fundo e
was indicative of well-preserved environmental conditions and is água superficial do rio Murucupi em Barcarena no estado do Pará. Dissertação
thus an indicator of good water quality. de Mestrado. Universidade Federal do Pará.
Garzio, L.M., Steinberg, D.K., 2013. Microzooplankton community composition along
the Western Antarctic Peninsula. Deep Sea Res. I Oceanogr. Res. Pap. 77, 36–49,
http://dx.doi.org/10.1016/j.dsr.2013.03.001.
5. Conclusion Gregório, A.M.D.S., Mendes, A.C., 2009. Characterization of sedimentary deposits
at the confluence of two tributaries of the Pará River estuary (Guajará Bay,
Our study on the Arapiranga, Curuperê-Dendê, and Murucupi Amazon). Cont. Shelf Res. 29, 609–618, http://dx.doi.org/10.1016/j.csr.2008.09.
007.
rivers shows that the effluents derived from domestic activities
Haberman, J., Haldna, M., 2014. Indices of zooplankton community as valuable
influence the population dynamics of the zooplankton community tools in assessing the trophic state and water quality of eutrophic lakes: long
structure (composition and density of species), which is different term study of Lake Võrtsjärv. J. Limnol. 73, 263–273, http://dx.doi.org/10.4081/
in each river. jlimnol.2014.828.
Heerkloss, R., Schnese, W., 1999. A long-term series of zooplankton monitoring of
According to the results from IndVal, Keratella lenzi and Anu- a shallow coastal water of the southern Baltic. Limnol. – Ecol. Manage. Inland
raeopsis sp1 proved to be potential bioindicators of waters affected Waters 29, 317–321, http://dx.doi.org/10.1016/S0075-9511(99)80021-8.
by eutrophication, while Difflugia distenda and Difflugia sp7 are INMET, 2014. Instituto Nacional de Meteorologia [WWW Document]. http://www.
inmet.gov.br/ (accessed 08.12.14).
potential bioindicators of well-preserved environments. These Ji, G., Wang, X., Wang, L., 2013. Planktonic rotifers in a subtropical shallow lake:
species may be used in additional studies to evaluate water quality succession, relationship to environmental factors, and use as bioindicators. Sci.
in rivers close sources of domestic or industrial effluents. World J. 201, 3, http://dx.doi.org/10.1155/2013/702942.
Jiang, Z., Huang, Y., Xu, X., Liao, Y., Shou, L., Liu, J., Chen, Q., Zeng, J., 2010. Advance
Nevertheless, the presence of these species indicates that the in the toxic effects of petroleum water accommodated fraction on marine
discharge of untreated domestic and sanitary effluents is the proba- plankton. Acta Ecol. Sin. 30, 8–15, http://dx.doi.org/10.1016/j.chnaes.2009.12.
ble source of changes in zooplankton community structure in areas 002.
Legendre, L., Legendre, P., 2012. Numerical Ecology. Elsevier, Amsterdam.
studied. According to these results, the Curuperê, Dendê, and Muru- Lima, M.d.O., 2011. Impactos Ambientais na Bacia Hidrográfica do Rio Pará: Uma
cupi drainages are already in advanced stages of environmental abordagem analítica e Quimiométrica. Tese de Doutorado. Universidade Federal
degradation, with compromised water quality. This highlights that do Pará.
Lima, M.d.O., Alves, F.A.d.S., Carneiro, B.S., Costa, V.B.d., 2009. Caracterização prelimi-
there is an immediate need for the construction of residue treat-
nar dos impactos ambientais, danos ao ecossitema e riscos a saúde decorrentes
ment systems, as well as the environmental recovery of the affected do lançamentos no rio Murucupi de efluentes do processo de beneficiamento de
rivers. Additionally, these results emphasize the exceptional envi- bauxita, Barcarena-Pará. Belém.
ronmental quality of Arapiranga River, which must be preserved. Madoni, P., 1994. A sludge biotic index (SBI) for the evaluation of the biological
performance of activated sludge plants based on the microfauna analysis. Water
Res. 28, 67–75, http://dx.doi.org/10.1016/0043-1354(94)90120-1.
Magalhães, A., Nobre, D.S.B., Bessa, R.S.C., Pereira, L.C.C., Costa, R.M., 2011. Seasonal
Acknowledgments and short-term variations in the copepod community of a shallow Amazon
estuary (Taperaçu, Northern Brazil). J. Coast. Res., 1520–1524.
The authors express their gratitude to the Conselho Maitra, P., 2011. Globalization of capitalism, agriculture and the negation. Int. J. Soc.
Econ. 24, 237–254.
Nacional de Desenvolvimento Científico e Tecnológico (CNPQ), Marale, S.M., 2012. Shifting role of ecology in solving global environmental prob-
IEC/FIDESA/MPE-PA (Process 001/2007), Federal University of Pará lems: selected practical tools. Environ. Dev. Sustain. 14, 869–884, http://dx.doi.
& Evandro Chagas Institute for funding the work and for providing org/10.1007/s10668-012-9362-8.
Marneffe, Y., Descy, J., Thome, J., 1996. The zooplankton of the lower river Meuse,
laboratory support for the research. Belgium: seasonal changes and impact of industrial and municipal discharges.
Hydrobiologia 319, 1–13.
May, L., O’Hare, M., 2005. Changes in Rotifer species composition and abundance
References along a trophic gradient in Loch Lomond, Scotland, UK. Hydrobiologia 546,
397–404, http://dx.doi.org/10.1007/s10750-005-4282-3.
APHA (American Public Health Association), AWWA (American Water Works Asso- Mclusky, D.S., 1989. The Estuarine Ecosystem. Chapman & Hall, London.
ciation), WEF (Water Environment Federation), 2012. Standard Methods for the Moon, C.H., Lee, Y.S., Yoon, T.H., 1994. Variation of trace Cu, Pb, and Zn in sediment
Examination of Water and Wastewater, 22 ed. American Public Health Associa- and water of an urban stream resulting from domestic effluents. Water Res. 28,
tion, Washington, DC. 985–991.
ASTM E1200-87(2012), 2012. Standard Practice for Preserving Zooplankton Sam- Moraes, B.C., De Maria, J., Carlos, A., Costa, M.H., 1998. Variação espacial e temporal
ples. ASTM International, West Conshohocken, PA, http://dx.doi.org/10.1520/ da precipitação no estado do Pará. Acta Amaz. 35, 207–214.
E1200-87R12.2. Moraitou-Apostolopoulou, M., Ignatiades, L., 1980. Pollution effects on the
Benndorf, J., Kranich, J., Mehner, T., Wagner, A., 2001. Temperature impact on the phytoplankton–zooplankton relationships in an inshore environment. Hydro-
midsummer decline of Daphnia galeata: an analysis of long-term data from the biologia 266, 259–266.
B.N.S. Costa et al. / Ecological Indicators 61 (2016) 526–545 545

Navarro, M.A.B., Modenutti, B.E., 2012. Precipitation patterns, dissolved organic Silva, C.E., 2011. Foraminíferos, Tecamebas e Bactérias Bentônicas na Praia de Encan-
matter and changes in the plankton assemblage in Lake Escondido tadas (Ilha do Mel, Paraná, Brasil) e a Possível Influência do Afluxo do Turístico
(Patagonia, Argentina). Hydrobiologia 691, 189–202, http://dx.doi.org/10.1007/ sobre esses organismos. Universidade Federal do Paraná.
s10750-012-1073-5. Silva, L.M.d., Silveira, G.L., 2006. Avaliação ambiental de sistema simplificado de
Oboh, I., Aluyor, E., Audu, T., 2009. Biosorption of heavy metal ions from aqueous esgotos.pdf. Rev. Bras. Recur. Hídricos 11, 85–98.
solutions using a biomaterial. Leonardo J. Sci. 8, 58. Smith, H.A., Burns, A.R., Shearer, T.L., Snell, T.W., 2012. Three heat shock proteins are
Panosso, R., Carlsson, P., Kozlowsy-Suzuki, B., Azevedo, S.M.F.O., Granéli, E., 2003. essential for rotifer thermotolerance. J. Exp. Mar. Biol. Ecol. 413, 1–6, http://dx.
Effect of grazing by a neotropical copepod, Notodiaptomus, on a natural doi.org/10.1016/j.jembe.2011.11.027.
cyanobacterial assemblage and on toxic and non-toxic cyanobacterial strains. Souza, C.A.d., 2014. Qualidade Ambiental de Recursos Hídricos Associados a Pivôs-
J. Plankton Res. 25, 1169–1175, http://dx.doi.org/10.1093/plankt/25.9.1169. Centrais de Irrigação no Distrito Federal. Dissertação de Mestrado. Universidade
Park, G.S., Marshall, H.G., 2000. Estuarine relationships between zooplankton com- de Brasília.
munity structure and trophic gradients. J. Plankton Res. 22, 121–135. Uriarte, I., Villate, F., 2004. Effects of pollution on zooplankton abundance and dis-
Perbiche-Neves, G., Fileto, C., Laço-portinho, J., Troguer, A., Serafim-Júnior, M., 2013. tribution in two estuaries of the Basque coast (Bay of Biscay). Mar. Pollut. Bull.
Relations among planktonic rotifers, cyclopoid copepods, and water quality in 49, 220–228, http://dx.doi.org/10.1016/j.marpolbul.2004.02.010.
two Brazilian reservoirs. Lat. Am. J. Aquat. Res. 41, 138–149. Utermöhl, H., 1958. Vervolkommung der quantitativen phytoplankton-methodik.
Pinheiro, S.C.C., Magalhães, A., da Costa, V.B., Pereira, L.C.C., da Costa, R.M., 2013. Mitteilungen Int. Vereiningung fuer Theor. und Angew. Limnol. 9, 1–9.
Temporal variation of zooplankton on a tropical Amazonian beach. J. Coast. Res., Van Gestel, C.A.M., Van Brummelen, T.C., 1996. Incorporation of the biomarker
1838–1843, http://dx.doi.org/10.2112/SI65-311.1. concept in ecotoxicology calls for a redefinition of terms. Ecotoxicology 5,
Pressler, N.G.d.S., 2005. Da Ação social a relação social: estudos das práticas de 217–225.
comunicação no complexo Industrial de Barcarena. Dissertação de Mestrado. Von Sperling, M., 2009. Princípios de Tratamento Biológico de Águas Residuárias:
Universidade Federal do Pará. Introdução à qualidade das águas e ao tratamento de esgostos, 4 ed. Departa-
Rocchetta, I., Pasquevich, M.Y., Heras, H., Ríos de Molina, M. del C., Luquet, C.M., mento de Engenharia Sanitária e Ambiental, Belo Horizonte.
2014. Effects of sewage discharges on lipid and fatty acid composition of the Wen, X.-L., Xi, Y.-L., Qian, F.-P., Zhang, G., Xiang, X.-L., 2010. Comparative analysis of
Patagonian bivalve Diplodon chilensis. Mar. Pollut. Bull. 79, 211–219, http://dx. rotifer community structure in five subtropical shallow lakes in East China: role
doi.org/10.1016/j.marpolbul.2013.12.011. of physical and chemical conditions. Hydrobiologia 661, 303–316, http://dx.doi.
Santos, E.C., de, O., Brabo, E.d.S., Sá, L.L.C., Lima, M.D.O., Girard, R.P., 2003. Relatório org/10.1007/s10750-010-0539-6.
Técnico da Avaliação da Mortandade de Peixes no Rio Murucupi Ocorrida no Yin, Y., Zhang, Y., Liu, X., Zhu, G., Qin, B., Shi, Z., Feng, L., 2011. Temporal and spatial
dia 04/04/03, no Município de Barcarena. Relatório Técnico. Instituto Evandro variations of chemical oxygen demand in Lake Taihu, China, from 2005 to 2009.
Chagas. Hydrobiologia 665, 129–141, http://dx.doi.org/10.1007/s10750-011-0610-.

View publication stats

You might also like