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Egyptian Journal of Aquatic Research 44 (2018) 195–202

Contents lists available at ScienceDirect

Egyptian Journal of Aquatic Research


journal homepage: www.sciencedirect.com/locate/ejar

Quality of the aquatic environment and diversity of benthic


macroinvertebrates of high Andean wetlands of the Junín region, Peru
María Custodio a,⇑, Fernán Chanamé a, Samuel Pizarro b, Danny Cruz a
a
Universidad Nacional del Centro del Perú, Instituto de Investigación en Alta Montaña, Av. Mariscal Castilla N 3989-4089, Huancayo, Peru
b
Universidad Nacional Agraria La Molina, Av. La Molina s/n La Molina, Casilla Lima 12, Lima, Peru

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

Article history: The objective of this study was to evaluate the quality of the aquatic environment and diversity of benthic
Received 25 January 2018 macroinvertebrates of high Andean wetlands in the Junín region, Peru, between March and December
Revised 10 August 2018 2017. Samples of water and benthic macroinvertebrates were collected from 22 sampling sites during
Accepted 20 August 2018
the rainy season and low water. The physical-chemical indicators of water quality determined in situ
Available online 6 September 2018
were: DO, DTS, EC, temperature and pH. The results obtained reveal that the physical-chemical and bac-
teriological indicators are within the environmental quality standards for water, except COD and BOD5.
Keywords:
Regarding the benthic macroinvertebrates, four phyla were identified, the most representative being
high Andean wetlands
Water quality
the phylum Arthropoda in abundance and taxa richness. Therefore, according to the sampling period,
Benthic macroinvertebrates highly significant differences were detected (p < 0.01) for conductivity, COD, temperature, nitrates and
Diversity thermotolerant coliforms, and significant differences (p < 0.05) for DTS. According to the wetland, 100%
of the indicators showed high significant differences. In addition, 70% of the indicators presented inter-
action according to sampling season and wetland. The greatest abundance and dominance were recorded
in the Tragadero wetland and the greater richness, diversity and equitability of taxa in the Pomacocha
wetland.
Ó 2018 National Institute of Oceanography and Fisheries. Hosting by Elsevier B.V. This is an open access
article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Introduction due to the cumulative effects of economic development (Noble


et al., 2011; Ball et al., 2013). These changes have generated in
High Andean wetlands are fragile – Multifunctional ecosystems recent decades the need to evaluate and better manage the direct,
with a high degree of environmental heterogeneity (Guswa et al., indirect and potentially induced effects on wetlands (Burgin, 2010;
2014). This complexity is favored by the diverse interactions and Wohl et al., 2015).
transitions between climate, geomorphology, precipitation, water Developed countries who are aware that the permanence and
flow and its river’s systems (Alvial et al., 2012). However, the quality of water are factors that affect the functioning of ecosys-
health of these ecosystems is affected by various anthropogenic tems, have implemented water policies in their legislation (Liu
pressures (Van Ael et al., 2015; Chapman et al., 2016) both in their et al., 2012). In Europe, Strategic Framework Directives such as
structure and in the services they provide; groundwater recharge, the Water Framework, Basin and Marine Water Quality Directive
water retention of flood, contributions of base flow, biogeochemi- have been implemented in 2000 (WFD, 2000/60/EC), 2006 (QBWD,
cal processing, improvement of water quality and wildlife habitat 2006/7/EC) and 2008 (MSFD, 2008/56/EC), respectively (Petus
(Jackson et al., 2016). et al., 2014). While in developing countries, water supply and
The increasing deterioration that these ecosystems are experi- treatment are the most important issues and account for the
encing due to pollution problems is leading to their degradation majority of investments in water management (Perrin et al.,
both globally and in basins (Quesnelle et al., 2015). At the global 2014). However, in practice, <20% of all wastewater effluents are
level, the extent of wetlands, especially in South Asia and South treated before being discharged to water bodies (Alvarez-Mieles
America, has fallen by 6% in just 14 years (from 1993 to 2007) et al., 2013).
Peru is a country with a strategic location for water resources,
but like many other countries, it faces problems of water availabil-
Peer review under responsibility of National Institute of Oceanography and
Fisheries. ity due to the growth of population densification and pollution
⇑ Corresponding author. problems (Eda and Chen, 2010). The projections of future water
E-mail address: mcustodio@uncp.edu.pe (M. Custodio).

https://doi.org/10.1016/j.ejar.2018.08.004
1687-4285/Ó 2018 National Institute of Oceanography and Fisheries. Hosting by Elsevier B.V.
This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
196 M. Custodio et al. / Egyptian Journal of Aquatic Research 44 (2018) 195–202

shortages in the tropical Andes of the world are increasingly alarm- lands are used for intensive cultivation of Oncorhynchus mykiss,
ing. The models forecast water deficits for decades of the future in Ñahuinpuquio for boat tourism and Tragadero for bird tourism.
this part of the South American continent, where the recession of In these latter two wetlands, urban expansion in the surrounding
the glaciers is a great concern. However, conflicts have already area is predominant and therefore the generation of urban
arisen in some Peruvian river basins, not only because of the prob- wastewater (Fig. 1).
lem of water availability and the contraction of alpine-type wet-
lands (Bury et al., 2013; Bury et al., 2013; Bury et al., 2013) but Collection of water sample and physical-chemical and bacteriological
also because of the great alterations that are causing the anthro- analysis
pogenic pollutants.
The biological evaluation of water quality has been imple- Water samples and benthos were collected at 22 sampling sites,
mented for many years complementing the physical-chemical during the rainy season in the high Andes (January, February,
indicators, with the benthic macroinvertebrates being the most March and April) and the dry season (May, June, July and August).
frequently used groups, since they offer a range of responses to dif- The physical-chemical indicators determined in situ in each wet-
ferent degrees of environmental stress throughout the time land were: dissolved oxygen (mg/l), total dissolved solids (mg/l),
(Nguyen et al., 2014; Sundermann et al., 2015; Pacioglu and conductivity (mS/cm), temperature (°C) and pH. These determina-
Moldovan, 2016). The use of benthic macroinvertebrates to assess tions were made directly in the waters of each sampling site, using
the ecological status of water bodies has become one of the main Hanna Instruments portable equipment. Also, water samples were
components of water-related legislation around the world collected at a depth of 20 cm in sterile glass jars; previously
(Couceiro et al., 2012; Lewin et al., 2014; Melo et al., 2015; labeled, treated with a 1:1 hydrochloric acid solution and rinsed
MacEdo et al., 2016), generally through several indices, many of with distilled water, for bacteriological, nitrate, total phosphorus,
them are based on taxa richness, as the simplest and most common COD and BOD5 analyses. On-site determinations of physical-
measure of biodiversity (Ramos-Merchante and Prenda, 2017). chemical indicators and collection of water samples were per-
Overall, the quality of the aquatic environment of freshwater formed by quadrupling at each sampling site. The preservation
wetlands has not received attention proportional to the wide dis- and transport of water samples to the laboratory for further anal-
tribution of this type of ecosystem. Further, at present, the ysis were carried out according to the standard method (APHA/
response of benthic macroinvertebrates to different environmental AWWA/WEF, 2012).
stressors is a widespread practice for evaluating the quality of The determination of thermotolerant coliforms was performed
water and habitat. Hence, a more integrated knowledge of the var- using the method of the most probable number by the multiple
ious processes of wetlands is necessary to make judgments about tube dilution technique. The biological oxygen demand (BOD5)
the likely effects of a series of impacts. In this sense, the present was determined using the Respirometric method with the OxiDir-
study has as general objective, to evaluate the quality of the aqua- ect Lovibond equipment. Nitrates (mg/L) and phosphates (mg/L)
tic environment and diversity of benthic macroinvertebrates of were determined with the PC-MultiDirect photometer, according
high Andean wetlands of the Junín region, Peru, between March to the procedure accepted by the United States Environmental Pro-
and December of 2017. tection Agency (USEPA, 1983).
Benthic macroinvertebrate collections
The collection of sediment for benthic macroinvertebrates was
Materials and methods carried out at the sites defined by the Hydro-Bios Ekman-Birge
dredge. One kilogram of sediment was collected from each sam-
Study area pling site. Next, 5% formaldehyde was added to each of the samples
for preservation and subsequent identification in the laboratory.
The Mantaro river basin is located in the Central Andes of Peru, Taxonomic identification of benthic macroinvertebrates was per-
between latitudes: 10° 340 S–13° 350 S and longitudes: 73° 550 W– formed at the family level through a trinocular stereomicroscope.
76° 400 W. The Pomacocha wetland is located in the area that goes Finally, the identified benthic macroinvertebrates were fixed with
to Comas at an altitude of 4543 m above sea level (18L 70% alcohol and form part of the water macrofauna collection of
472578.8928E 8697395.1004N), Cuncancocha in the area that goes the Water Research Laboratory (Huamantinco and Ortiz, 2010).
to the Nor Yauyos Cochas landscape reserve at 4503 m above sea
level (18L 489222.4805E 8668292.9936N), Incacocha and Ñahuin-
puquio located in the province of Chupaca at 4425 masl (18L Analysis of data
417879.0000E 8669608.0000N) and 3379 masl (18L
463170.9300E 8665411.6800N), respectively, and Tragadero In order to evaluate the quality of the aquatic environment with
located in the province of Jauja at 3471 masl (18L 441749.7040E adequate efficiency, the surface water quality and the diversity of
8698909.4474N). The vegetation in these ecosystems is very diver- taxa of benthic macroinvertebrate communities were determined.
sified herbaceous, both in temporary and permanent species, with To do this, multivariate statistical methods were used, such as mul-
erect and stunted growth, and very particular and specific morpho- tiple variance analysis (MANOVA), correlation analysis and cluster
logical characteristics. The most representative families are Poa- analysis (Everitt et al., 2011).
ceae, Asteraceae, Cyperaceae, Plantaginaceae, Caryophyllaceae,
Apiaceae, Geraniaceae, Ranunculaceae, Gentianaceae, Rosaceae, Multiple variance analysis
Isoetaceae, Polygonaceae, Fabaceae, Oxalidaceae and Juncaceae.
The productive activities in the high Andean wetlands are asso- To detect the difference between physical-chemical indicators
ciated with the altitudinal floor. In the Puna, Jalca and Moor areas, between wetlands, the generalized linear model was used by mul-
the predominant activities are: cattle, sheep and camelid cattle tiple variance analysis without interaction for electrical
raising, mining and fishing. As subsistence activity is the extraction conductivity-EC, biochemical oxygen demand-BOD5 and dissolved
of plants and peat as fuel, since a large part of the rural population total solids-DTS; and with interaction for the variables pH, chemi-
depends on firewood for cooking their food. At lower altitudes, cal oxygen demand-COD, dissolved oxygen-DO, temperature,
potato and other tuber crops and Andean cereals are grown. The nitrates and total phosphorus. The model was decided according
water bodies of the Pomacocha, Incacocha and Cuncancocha wet- to the significance or not of the interactions, being:
M. Custodio et al. / Egyptian Journal of Aquatic Research 44 (2018) 195–202 197

Fig. 1. Location of water sampling sites and benthic macroinvertebrates in high Andean wetlands.

vffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
Model without interaction u p
uX
dðx; yÞ ¼ t ð xi  y i Þ 2
i¼1

Yijk ¼ l þ Li þ Tj þ eijk

where: Yijk ¼EC, BOD5 and DTS, l ¼General average, Li ¼ Wetland Calculation of biodiversity indicators
effect, Tj ¼Effect of time (dry and rain) and eijk ¼Error.
The diversity of benthic macroinvertebrate communities of high
Model with interaction
Andean wetlands was calculated by means of multiple metrics
Yijk ¼ l þ Li þ Tj þ ðL  TÞij þ eijk based on abundance, richness, dominance of Simpson, Shannon-
Weiner (H’), Margalef and equity of Pielou at the family level.
Where: Yijk ¼pH, COD, DO, temperature, nitrates and total phospho- The calculations were made with the Past program (version 3.0).
rus, l ¼General average, Li ¼ Wetland effect, Tj ¼Effect of time (dry
and rain), ðL  TÞij = Effect of interaction between wetland and season
Results
and eijk ¼ Error

Physico-chemical and bacteriological quality of water


Correlation analysis
Table 1 shows the descriptive statistics of the physical-chemical
The Pearson correlation coefficients were calculated with the
and bacteriological indicators of the water quality of high Andean
statistical software Statgraphics Centurion version XVI.II, using
wetlands, considering the sampling period. The pH of the water
logarithmically transformed data for the indicators of biodiversity
presented variations in each of the evaluated wetlands, with values
of benthic macroinvertebrates. Significant or highly significant
that ranged from 5.88 in the Cuncancocha wetland to 8.91 in the
positive or negative correlations were assumed when the p-
Incacocha wetland, during the dry season. However, these varia-
calculated value was <0.05 or 0.01, respectively.
tions are within the natural ranges for aquatic life, the production
P P
P ð XÞð YÞ of drinking water and other uses, according to the environmental
XY 
r ¼ sffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
 P 
n
P 
quality standards for water of the Ministry of Environment of Peru
P 2 ð XÞ2 P 2 ð YÞ2 (MINEN, 2015). As well as, within the ranges established by the
X  n Y  n
World Health Organization (6.5–8.5) (Agency Protection, 2013)
and the Canadian Council of Ministers of the Environment (Cana-
dian Council of Ministers of the Environment (6.5–9.0) (CCME,
Cluster Analysis 2007). Similar behavior showed the electrical conductivity, observ-
ing the greater variation in the wetland of Ñahuinpuquio in both
In this study, hierarchical agglomeration was performed in the sampling seasons.
standardized benthic macroinvertebrate biodiversity indicator The average values of the chemical demand for oxygen-COD
data set using the Ward method, using Euclidean distances as a were higher than the environmental quality standards (EQS), cate-
measure of similarity (Everitt et al., 2011). gory 3 (40 mg/l) in the Tragadero and Cuncancocha wetlands in
198 M. Custodio et al. / Egyptian Journal of Aquatic Research 44 (2018) 195–202

both rainy and dry season, reaching a maximum value of 60.50


(mg/l) in the Tragadero wetland. While the BOD5 recorded in all
6.5–9.0
MINEN

the studied wetlands far exceeded the EQS (10 mg/l). The lowest

1000.0

1000.0
(2015)

25.0

0.036
▲3.0
5.0

13.0
40.0
EQS

dissolved oxygen concentrations were recorded in the Tragadero

5.0
wetland during the dry season. The average temperature values
252.84 ± 43.79
ranged between 9.28 °C in the Ñahuinpuquio wetland and

23.00–19.70

35.00–23.00
36.00–30.00
33.81 ± 1.35

26.00 ± 3.75
20.70 ± 0.84
325–193.50

19.46 °C in Tragadero, both in the dry season, a behavior that

10.00–8.40
7.32 ± 0.24

9.28 ± 0.38

2.35 ± 0.43
7.74 ± 0.09

1.48 ± 0.02
0.76 ± 0.01
7.62–6.65

1.55–1.45
7.90–7.60

0.78–0.73
3.00–2.00
would be due to the differences in the sampling time and the ambi-
ent temperature.
Dry

The highest values of total dissolved solids-DTS were registered


258.77 ± 37.89

in the Tragadero wetland, ranging between 12.50 mg/l and


37.30–33.00

22.00–19.50

35.00–23.00
24.75 ± 3.42
34.52 ± 1.01

10.61 ± 0.34
20.80 ± 0.72

11.20–9.60
12.60 mg/l. The mean values of total phosphorus were higher than
7.63 ± 0.13

7.12 ± 0.15

2.75 ± 0.28

1.55 ± 0.05
0.74 ± 0.02
1.75–1.45
7.80–7.20

7.40–6.80

0.76–0.69
3.00–2.00
320–200

the EQS of Peru (0.035 mg/l), in all the wetlands under study, espe-
Rain
Descriptive statistics on the physical-chemical and bacteriological indicators of water quality in high Andean wetlands and environmental quality standards for water, category IV-Peru.

cially in the Tragadero wetland, which has values that are triple the
concentrations of the other wetlands. The highest average nitrate
Ñahuinpuquio

250.75 ± 5.01

values were found in the Tragadero wetland. However, the concen-


38.00–36.50

20.50–16.60

23.00–22.00
37.17 ± 0.46

18.41 ± 0.93

22.42 ± 0.50
10.00–8.40
9.28 ± 0.38

2.51 ± 0.39

1.31 ± 0.49
8.86 ± 0.05

6.38 ± 0.05

0.50 ± 0.05
8.91–8.76

6.56–6.33

2.12–0.55
0.56–0.44
3.00–2.00

trations of thermotolerant coliforms registered in all the wetlands


265–240

did not surpass the EQS of Peru (1000 NMP/100 ml).


Dry

Table 2 shows the results of the multiple variance analysis of


the physical-chemical and bacteriological indicators with and
262.53 ± 4.67

2.63 ± 0.0.34

26.00–23.00
40.00–38.00

20.00–18.00

23.86 ± 1.39

without interaction, considering sampling season and wetland.


38.83 ± 0.82

18.51 ± 0.57

10.51 ± 0.43
271.50–250

11.20–9.60
8.61 ± 0.24

6.43 ± 0.09

1.51 ± 0.04
0.50 ± 0.05
Incacocha

1.62–1.42
6.70–6.25

0.56–0.43
8.90–8.00

3.00–2.00

According to the sampling period, highly significant differences


were detected (p < 0.01) for conductivity, COD, temperature,
Rain

nitrates and thermotolerant coliforms, and significant differences


(p < 0.05) for total dissolved solids. According to the wetland,
252.19 ± 2.88
46.00–45.00

35.00–22.00
10.70–10.00
20.00–10.00

24.42 ± 2.72
45.39 ± 0.41

18.44 ± 2.70

10.52 ± 0.19

0.47 ± 0.004

100% of the indicators showed highly significant differences. In


6.79 ± 0.53

6.38 ± 0.25

2.36 ± 0.38

0.79 ± 0.01
258–248.4
7.70–5.88

6.70–5.55

0.81–0.79

0.47–0.46
3.00–2.00

addition, 70% of the indicators presented interaction according to


sampling season and wetland.
Dry

In the indicator wetland interaction (p < 0.01) the highest aver-


260.35 ± 5.16

age pH values were recorded in the Incacocha wetland, followed by


Cuncancocha

12.30–10.60
55.00–45.00

26.00–22.00
20.00–17.00
59.64 ± 1.02

11.38 ± 0.44
18.68 ± 0.90

0.46 ± 0.004
270.60–250

23.5 ± 1.53
7.16 ± 0.24

2.58 ± 0.17
6.50 ± 0.22

0.80 ± 0.03

Ñahuinpuquio and Tragadero. However, these pH values did not


7.50–6.55

7.00–5.91

0.87–0.75

0.47–0.46
3.00–2.30

exceed the EQS for water in any of their categories. For the COD,
Rain

the effect was also detected according to the sampling period


(p < 0.01), wetland (p < 0.01) and interaction (p < 0.01). The highest
264.34 ± 16.21

440.00–35.00

average values of COD were recorded in Tragadero followed by


211.6 ± 146.3
21.70–18.40
58.30–55.00

30.50–26.90
28.43 ± 0.91

19.46 ± 0.93
56.49 ± 0.80

12.60–6.00
9.24 ± 1.73
7.53 ± 0.55

6.02 ± 0.24

1.49 ± 0.02

0.76 ± 0.06
325.6–252

Cuncancocha, values that exceeded the EQS (40.00 mg/l). For the
6.42–5.45

1.56–1.47
8.10–6.56

0.87–0.66

dissolved oxygen, an effect was also detected by the wetland factor


Dry

(p < 0.01) and in the interaction (p < 0.01). The Tragadero wetland
presented the mean dissolved oxygen values close to the limit
465.8 ± 171.7

value of the EQS, revealing processes that deteriorated the water


60.50–55.90

30.50–26.70

18.50–17.00
28.81 ± 1.12
59.64 ± 1.02

17.70 ± 0.38
12.50–7.50
9.20 ± 1.34
7.56 ± 0.41

6.12 ± 0.10

1.52 ± 0.04

0.77 ± 0.04
269 ± 8.25
Tragadero

1.62–1.44
8.30–6.85

0.85–0.68
6.30–6.00

quality. For temperature, MANOVA also detected highly significant


285–260

710–150

differences for sampling season (p < 0.01), wetland (p < 0.01) and
Rain

interaction (p < 0.01), with the Tragadero wetland presenting the


highest values. For the total phosphorus indicator, only highly sig-
248.17 ± 6.54
34.00–28.30

14.50–10.40
20.00–16.50

26.00–22.00
11.55 ± 1.27

23.41 ± 1.43
30.58 ± 1.31

18.08 ± 0.73

nificant differences were detected for wetland (p < 0.01) and inter-
6.63 ± 0.21

2.86 ± 0.34
6.80 ± 0.14

0.41 ± 0.05
0.04 ± 0.01
258.2–222
7.18–6.48

7.04–5.56

3.60–2.00

0.50–0.34
0.06–0.03

action (p < 0.01), observing a wide range between the Pomacocha


and Tragadero wetland. While the nitrate indicator showed highly
Dry

significant differences for sampling period (p < 0.01), wetland


(p < 0.01) and interaction (p < 0.01).
24.86 ± 1.475
254.18 ± 4.52

13.60–10.70
33.50–30.00

19.00–17.00

26.00–23.00
11.74 ± 0.77
31.10 ± 0.98

18.07 ± 0.49
Pomacocha

6.83 ± 0.18

6.68 ± 0.12

3.10 ± 0.21

0.04 ± 0.01

0.40 ± 0.03

Pomacocha and Ñahuinpuquio were the wetlands with the


7:00–6.44
7.82–6.58

3.60–2.56

0.49–0.36
0.06–0.03
262–250

greatest similarities to the similarity cluster analysis. While the


Rain

Tragadero wetland does not have a marked similarity with the


other wetlands studied, revealing the quality of the water deterio-
rated by the high concentrations of the physical-chemical indica-
Descriptive

Mean ± SD

Mean ± SD

Mean ± SD

Mean ± SD

Mean ± SD

Mean ± SD

Mean ± SD

Mean ± SD

Mean ± SD

Mean ± SD

tors detected. However, this wetland is conglomerated with the


statistics

Cuncancocha wetland, which shows signs of organic contamina-


Rank

Rank

Rank

Rank

Rank

Rank

Rank

Rank

Rank

Rank

tion, due to the high concentrations of BOD5 that exceed the EQS
of Peru.
Thermotolerant coliforms
Dissolved oxygen (mg/l)

Total phosphorus (mg/l)

Patterns of abundance, richness and diversity of benthic


Temperature (°C)

(MLN/100 ml)

macroinvertebrates
Nitrates (mg/l)
BOD5 (mg/l)
COD (mg/l)
EC (mS/cm)

DTS (mg/l)

Four phyla, six classes, nine orders and 14 families of benthic


Indicator

macroinvertebrates were identified in five high Andean wetlands


Table 1

pH

of the Junín region, during the rainy and dry seasons. The phylum
Arthropoda was the most representative in abundance and rich-
M. Custodio et al. / Egyptian Journal of Aquatic Research 44 (2018) 195–202 199

Table 2
Multiple variance analysis of the physical-chemical and bacteriological indicators with and without interaction, considering sampling season and wetland.

Indicator A: Season B: Wetland AxB


Rain Dry Sig. Pomacocha Tragadero Cuncancocha Incacocha Ñahuinpuquio Sig. Sig.
EC (mS/cm) 261.05b 253.94a **
251.18a 267.08b 256.77a 256.64a 255.80a **

BOD5 (mg/l) 20.96 20.82 n.s 18.08a 28.62d 18.56b 18.46ab 20.75c **

DTS(mg/l) 4.05b 3.86a *


2.98b 9.21c 2.47a 2.57a 2.55a **

pH 7.56 7.54 n.s 6.82a 7.55c 6.97b 8.73e 7.69d ** **

COD (mg/l) 42.19b 40.69a **


30.84a 58.06e 46.13d 38.00c 34.16b ** **

Dissolved oxygen (mg/l) 6.57 6.55 n.s 6.65c 6.07a 6.43b 6.40b 7.22d ** **

Temperature (°C) 12.38b 12.02a **


11.65c 18.59d 10.95b 9.90a 9.95a ** **

Total phosphorus (mg/l) 0.72 0.72 n.s 0.04a 1.51e 0.80d 0.50b 0.75c ** **

Nitrates (mg/l) 0.94b 0.89a **


0.40a 0.77c 0.47b 1.41d 1.52e ** **

Thermotolerant coliforms (MLN/100 ml) 112.56b 61.56a **


24.13a 338.71b 23.96a 23.15a 25.38a ** **

*
Significative effects (p < 0.05).
**
Highly significant effects (p < 0.01). Non-significant effects (n.s). Different letters represent significant differences according to the LSD test (p < 0.05).

Table 3
Abundance of taxa of benthic macroinvertebrates captured in the wetlands of Pomacocha (Pc), Tragadero (Tg), Cuncacococha (Cc), Incacocha (Ic) and Ñahuinpuquio (Ñq), in rainy
and dry seasons.

Phylum Class Order Family Abundance (N°. m2)


Rainy season Dry season
Pc Tg Cc Ic Ñq Pc Tg Cc Ic Ñq
Platyhelmintes Turbellaria Tricladida Dugesiidae 0 4 0 0 0 0 0 0 0 0
Planariidae 3 0 0 0 0 8 0 5 2 0
Annelida Oligochaeta Tubificida Tubificidae 6 17 3 6 2 9 9 6 4 5
Hirudinea Glossiphoniiformes Glossiphoniidae 0 0 0 0 0 2 10 2 0 0
Mollusca Gastropoda Basommatofora Lymnaeidae 0 23 0 0 0 7 13 4 0 3
Arthropoda Crustacea Amphipoda Hyalellidae 2 0 0 0 0 5 0 3 0 0
Insecta Ephemeroptera Baetidade 45 11 5 6 11 60 8 22 21 0
Leptophlebiidae 32 0 0 0 0 59 4 0 0 0
Trichoptera Psychomyiidae 7 0 0 0 0 23 0 0 0 0
Limnephilidae 13 0 6 7 5 17 0 7 8 5
Coleoptera Hydrophilidae 39 0 5 9 30 50 6 29 21 22
Diptera Ceratopogonidae 65 37 34 42 38 55 18 47 47 27
Chironomidae 135 314 61 84 83 462 336 81 93 95
Psychodidae 11 62 10 0 37 55 76 30 15 36

ness of taxa, with the Insecta class being the most distinctive with Tragadero wetlands, revealing the low values presented by the
88.89% of the total phylum taxa. The greatest number of individu- benthic macroinvertebrate diversity indices.
als of benthic macroinvertebrates was recorded in the Tragadero
wetland during both rainy and dry seasons and corresponded to
the order Diptera, family Chironomidae (Table 3). Relationships of the physical-chemical and bacteriological indicators
The highest average value of abundance (120.30 ± 21.30) was with the diversity of benthic macroinvertebrates of high Andean
recorded in the Tragadero wetland where specimens of the Chi- wetlands
ronomidae family predominated, followed by Pomacocha and Cun-
cancocha (116.00 ± 21.76 and 59.50 ± 23.20, respectively) during Table 4 shows the results of the multiple linear correlation anal-
the dry season. The highest taxa richness (7.71 ± 1.80) was ysis, using the Pearson coefficient for each pair of variables. It is
recorded in the Pomacocha wetland and the highest dominance observed that the correlation of the variables temperature and
(0.54 ± 0.07) in the Tragadero wetland. The diversity indices of total dissolved solids with the abundance of benthic macroinverte-
Simpson (1-D) and Shannon-Wiener (H ’) were higher in the Poma- brates are positive and highly significant (p < 0.01), while between
cocha wetland (0.74 ± 0.09, 1.57 ± 0.28, respectively) in the rainy nitrates and abundance the correlation is negative and significant
season. Similar behavior presented the mean values of Margalef (p < 0.05). Similar behavior of COD, total phosphorus and nitrates,
(1.41 ± 0.29) and Equitability (J) (0.84 ± 0.05), in this sampling when correlated with richness, show negative and high signifi-
period. cance (p < 0.01); and pH, conductivity, BOD5 and thermotolerant
Fig. 2 shows the grouping by similarity of the high Andean wet- coliforms, when correlated with richness, are negative and signifi-
lands evaluated by indicators of biodiversity of benthic macroin- cant. The correlation of COD, BOD5, total phosphorus and thermo-
vertebrates, in which it can be seen that wetlands are separated tolerant coliforms with the dominance of macroinvertebrates was
by increasing the abundance of indicator specimens from dis- positive and highly significant, while the correlation of conductiv-
turbed aquatic environments, especially where there is high avail- ity and total dissolved solids with dominance was positive and that
ability of organic matter. The wetlands that presented greater of dissolved oxygen with the dominance was negative, but signifi-
similarity were Pomacocha with Cuncancocha and Tragadero with cant. Also, COD and BOD5 and total phosphorus showed highly sig-
Incacocha. While the Ñahuinpuquio wetland is separated from the nificant correlations with the Margalef index. The correlation of
rest of the wetlands, but conglomerates with the Incacocha and BOD5, dissolved total solids and thermotolerant coliforms with
200 M. Custodio et al. / Egyptian Journal of Aquatic Research 44 (2018) 195–202

aerobic microorganisms that tend to accelerate organic matter


degradation processes by making use of the oxygen content of
the water (Ayandiran et al., 2018), as corroborated by the high
BOD5 concentrations recorded in these wetlands. Variations in
the mean dissolved oxygen values obtained indicate the interac-
tion of this gas with the atmosphere as well as the photosynthetic
and respiratory processes that occur in water (Kuzmanovic et al.,
2017). The high BOD5 values recorded in the five wetlands reveal
a high concentration of organic matter and thus a high demand
for oxygen for its degradation.
Temperature is a limiting factor for most aquatic organisms that
acquires great importance in the development of the different pro-
cesses that are carried out in water, such as the dissolution of oxy-
gen, since it determines the trend of its physical properties and the
Fig. 2. Grouping by similarity of high Andean wetlands evaluated by indicators of richness and distribution of aquatic biota (Seiler et al., 2015). The
biodiversity of benthic macroinvertebrates. data recorded in the wetlands evaluated show a uniform tempera-
ture, although higher in the Tragadero wetland, where high oxygen
demands were registered by the microbiota, which would be influ-
the Equitability (J) of benthic macroinvertebrate communities was
encing the water temperature. Phosphorus is one of the limiting
highly significant.
factors of the growth of algae and aquatic plants, so that the deter-
mination of its concentrations can detect problems of eutrophica-
tion of bodies of water (Cony et al., 2016). The average values
Discussion
obtained from total phosphorus in the evaluated wetlands exceed
the EQS (0.035 mg/L). In addition, these high phosphorus concen-
Physico-chemical and bacteriological quality of water
trations reveal the contamination events through which the wet-
land crosses due to the development of anthropogenic activities;
The demand for water for its different uses is increasing rapidly
among them the cattle activities, since the feces of the cattle are
in recent decades, exerting strong pressure on the availability of
a potential source of phosphorus.
this resource. The results of the pH of the water obtained reveal
a clear trend towards alkalinity, which would be related to the
edaphic conditions of wetlands, agricultural activity (Rim et al.,
2017) and wastewater discharges (Christia et al., 2014). Another Patterns of abundance, richness and diversity of benthic
factor that would be contributing to the pH variation of the water macroinvertebrates
would be the photosynthetic activity that occurs during the day
(Craft et al., 2017). The highest values of conductivity recorded The results obtained show that the most abundant benthic
during the dry season in the Tragadero wetland would be due to macroinvertebrates correspond to individuals of the class Insecta,
the presence of ions and anions that are concentrated due to evap- order Diptera. They also reveal differences between the communi-
oration and the processes of degradation of organic matter that ties of the five wetlands, with the Chironomidae family being the
accelerate the concentration of ions in the water (Effendi, 2016). most representative with a wide range in all zoogeographic regions
The dissolved oxygen together with the temperature determine (Vamosi et al., 2012). The abundance recorded in the Cuncancocha
the richness and distribution patterns of benthic macroinverte- wetland during the rainy season confirms the average level of oxy-
brate families (Lake et al., 2017). According to MINEN (2015), the genation of water bodies. Likewise, the greater abundance of these
conservation of the aquatic environment of wetlands classified in individuals registered in the Tragadero wetland confirms the low
category 2 of the environmental quality standards for water should level of oxygenation of their waters. These results coincide with
not have values of DO < 5 mg/L. However, the slightly low concen- those recorded in other studies in aquatic environments with
trations of DO recorded in the high Andean wetlands assessed dur- low oxygen levels, with dominance of Chironomidae and decrease
ing the rainy and low water periods would be related to the in macroinvertebrate density (Riens et al., 2013). However, these
anthropogenic activities that take place in these ecosystems, such effects are related to the decrease in water and food quality, as well
as the intensive cultivation of Oncorhynchus mykiss, the entry of as to the interference of breathing mechanisms and other morpho-
cattle to graze and domestic activities such as washing clothes physiological characteristics (Miserendino et al., 2012). Other fam-
and bathing of local people. These activities could be a source of ilies registered and important for their abundance in the high

Table 4
Relation of the physical-chemical and bacteriological indicators with the diversity of benthic macroinvertebrates of high Andean wetlands.

Physical-chemical and bacteriological indicators Abundance Richness Dominance Simpson Shannon Margalef Equitability (J)
pH -0.246 0.346* 0.121 0.121 0.178 0.189 0.056
EC (mS/cm) 0.251 0.316* 0.375* 0.375* 0.443** 0.127 0.297*
DQO (mg/l) 0.022 0.493** 0.403** 0.403** 0.432** 0.481** 0.233
DBO5 (mg/l) 0.238 0.345* 0.435** 0.435** 0.432** 0.404** 0.386**
Dissolved oxygen (mg/l) 0.282 0.205 0.357* 0.357* 0.318* 0.280 0.320*
Temperature (°C) 0.437** 0.018 0.285 0.285 0.258 0.105 0.357*
DTS (mg/l) 0.399** 0.094 0.346* 0.346* 0.285 0.167 0.405**
Total Phosphorus (mg/l) -0.005 0.535** 0.399** 0.399** 0.432** 0.478** 0.196
Nitrates (mg/l) 0.319* 0.476** 0.162 0.162 0.233 0.272 0.039
Thermotolerantcoliforms NMP/100 ml 0.100 0.353* 0.460** 0.460** 0.524** 0.309* 0.405**
*
significant correlations (p < 0.05).
**
highly significant correlations (p < 0.01).
M. Custodio et al. / Egyptian Journal of Aquatic Research 44 (2018) 195–202 201

Andean wetlands are Baetidae and Psychodidae, which are charac- Conflict of interest
terized by living in oligotrophic waters.
The highest abundance of individuals of the order Ephe- The authors declare that they have no conflict of interest.
meroptera was recorded in the Pomacocha wetland in both sam-
pling seasons. These results reveal that the great majority of Acknowledgements
species of this order have low tolerance to contamination
(Serrano Balderas et al., 2016). The Trichoptera order is an impor- The authors express our gratitude to the General Research Insti-
tant component of benthic communities and the basis of the tute of the National University of Central Peru for the financing of
trophic chain of aquatic ecosystems. The greatest abundance of the study, to the Water Research Laboratory for allowing us to
the order Trichoptera was recorded in the Pomacocha wetland, make use of the equipment and materials for this study.
where the quality of the water is good. The most representative
family for its abundance is Leptophlebiidae. These results are cor- Author contributions
roborated by Mereta et al. (2012), who point out that Trichoptera
are restricted to environments with vegetation, water depth and María Custodio developed the concept and design of the field
conductivity. The order Coleoptera is the taxon that has colonized study and wrote the manuscript. She conducted analyses of ben-
all aquatic environments evaluated. thic macroinvertebrate and thermotolerant coliform communities,
This study shows the positive and negative correlation, provided interpretation of the data and verified laboratory data-
significant and highly significant between the physical-chemical base. Fernán Chanamé carried out the determination of physical-
indicators and the indicators of diversity of benthic macroinverte- chemical parameters in situ and laboratory, Samuel Pizarro carried
brates. These results coincide with those of Verdonschot et al. out sediment sampling, compiled the data and elaborated the loca-
(2012) and Mykrä et al. (2012), who refer that in areas with a tion map of the wetlands under study, and Danny Cruz carried out
temperate climate, seasonality plays a very important role in the the statistical analysis and drafting of the results section. All
structure of macroinvertebrate communities. authors approved the final version before submission.
However, unlike the lotic systems, the altitudinal gradient has
not had a preponderant role, since the wetlands of Cuncancocha
and Pomacocha harbor the greatest wealth of macroinvertebrates,
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