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Microzooplankton as a bioindicator of
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Ecological Indicators 61 (2016) 526–545
Ecological Indicators
journal homepage: www.elsevier.com/locate/ecolind
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.
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
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)
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 (%)
October
November
December
June
May
August
March
September
January
February
July
Table 1
Water Quality Index in Arapiranga, Curuperê-Dendê, and Murucupi rivers in 2012.
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.
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.
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.
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
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.
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)
A1 A2 A3 A1 A2 A3 A1 A2 A3 A1 A2 A3
Table 5 (Continued)
A1 A2 A3 A1 A2 A3 A1 A2 A3 A1 A2 A3
Table 5 (Continued)
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
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.
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)
C1 C2 C3 C1 C2 C3 C1 C2 C3 C1 C2 C3
Table 6 (Continued)
C1 C2 C3 C1 C2 C3 C1 C2 C3 C1 C2 C3
Table 6 (Continued)
C1 C2 C3 C1 C2 C3 C1 C2 C3 C1 C2 C3
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.
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)
M1 M2 M3 M1 M2 M3 M1 M2 M3 M1 M2 M3
Table 7 (Continued)
M1 M2 M3 M1 M2 M3 M1 M2 M3 M1 M2 M3
Table 7 (Continued)
M1 M2 M3 M1 M2 M3 M1 M2 M3 M1 M2 M3
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
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