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

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

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-
ing. The models forecast water deficits for decades of the future in
this part of the South American continent, where the recession of
the glaciers is a great concern. However, conflicts have already
arisen in some Peruvian river basins, not only because of the prob-
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
also because of the great alterations that are causing the anthro-
pogenic pollutants.
The biological evaluation of water quality has been imple-
mented for many years complementing the physical-chemical
indicators, with the benthic macroinvertebrates being the most
frequently used groups, since they offer a range of responses to dif-
ferent degrees of environmental stress throughout the time
(Nguyen et al., 2014; Sundermann et al., 2015; Pacioglu and
Moldovan, 2016). The use of benthic macroinvertebrates to assess
the ecological status of water bodies has become one of the main
components of water-related legislation around the world
(Couceiro et al., 2012; Lewin et al., 2014; Melo et al., 2015;
MacEdo et al., 2016), generally through several indices, many of
them are based on taxa richness, as the simplest and most common
measure of biodiversity (Ramos-Merchante and Prenda, 2017).
Overall, the quality of the aquatic environment of freshwater
wetlands has not received attention proportional to the wide dis-
tribution of this type of ecosystem. Further, at present, the
response of benthic macroinvertebrates to different environmental
stressors is a widespread practice for evaluating the quality of
water and habitat. Hence, a more integrated knowledge of the var-
ious processes of wetlands is necessary to make judgments about
the likely effects of a series of impacts. In this sense, the present
study has as general objective, to evaluate the quality of the aqua-
tic environment and diversity of benthic macroinvertebrates of
high Andean wetlands of the Junín region, Peru, between March
and December of 2017.
Materials and methods
Study area
The Mantaro river basin is located in the Central Andes of Peru,
between latitudes: 10° 340 S–13° 350 S and longitudes: 73° 550 W–
76° 400 W. The Pomacocha wetland is located in the area that goes
to Comas at an altitude of 4543 m above sea level (18L
472578.8928E 8697395.1004N), Cuncancocha in the area that goes
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
417879.0000E 8669608.0000N) and 3379 masl (18L
463170.9300E 8665411.6800N), respectively, and Tragadero
located in the province of Jauja at 3471 masl (18L 441749.7040E
8698909.4474N). The vegetation in these ecosystems is very diver-
sified herbaceous, both in temporary and permanent species, with
erect and stunted growth, and very particular and specific morpho-
logical characteristics. The most representative families are Poa-
ceae, Asteraceae, Cyperaceae, Plantaginaceae, Caryophyllaceae,
Apiaceae, Geraniaceae, Ranunculaceae, Gentianaceae, Rosaceae,
Isoetaceae, Polygonaceae, Fabaceae, Oxalidaceae and Juncaceae.
The productive activities in the high Andean wetlands are asso-
ciated with the altitudinal floor. In the Puna, Jalca and Moor areas,
the predominant activities are: cattle, sheep and camelid cattle
raising, mining and fishing. As subsistence activity is the extraction
of plants and peat as fuel, since a large part of the rural population
depends on firewood for cooking their food. At lower altitudes,
potato and other tuber crops and Andean cereals are grown. The
water bodies of the Pomacocha, Incacocha and Cuncancocha wet-
lands are used for intensive cultivation of Oncorhynchus mykiss,
Ñahuinpuquio for boat tourism and Tragadero for bird tourism.
In these latter two wetlands, urban expansion in the surrounding
area is predominant and therefore the generation of urban
wastewater (Fig. 1).
Collection of water sample and physical-chemical and bacteriological
analysis
Water samples and benthos were collected at 22 sampling sites,
during the rainy season in the high Andes (January, February,
March and April) and the dry season (May, June, July and August).
The physical-chemical indicators determined in situ in each wet-
land were: dissolved oxygen (mg/l), total dissolved solids (mg/l),
conductivity (mS/cm), temperature (°C) and pH. These determina-
tions were made directly in the waters of each sampling site, using
Hanna Instruments portable equipment. Also, water samples were
collected at a depth of 20 cm in sterile glass jars; previously
labeled, treated with a 1:1 hydrochloric acid solution and rinsed
with distilled water, for bacteriological, nitrate, total phosphorus,
COD and BOD5 analyses. On-site determinations of physical-
chemical indicators and collection of water samples were per-
formed by quadrupling at each sampling site. The preservation
and transport of water samples to the laboratory for further anal-
ysis were carried out according to the standard method (APHA/
AWWA/WEF, 2012).
The determination of thermotolerant coliforms was performed
using the method of the most probable number by the multiple
tube dilution technique. The biological oxygen demand (BOD5)
was determined using the Respirometric method with the OxiDir-
ect Lovibond equipment. Nitrates (mg/L) and phosphates (mg/L)
were determined with the PC-MultiDirect photometer, according
to the procedure accepted by the United States Environmental Pro-
tection Agency (USEPA, 1983).
Benthic macroinvertebrate collections
The collection of sediment for benthic macroinvertebrates was
carried out at the sites defined by the Hydro-Bios Ekman-Birge
dredge. One kilogram of sediment was collected from each sam-
pling site. Next, 5% formaldehyde was added to each of the samples
for preservation and subsequent identification in the laboratory.
Taxonomic identification of benthic macroinvertebrates was per-
formed at the family level through a trinocular stereomicroscope.
Finally, the identified benthic macroinvertebrates were fixed with
70% alcohol and form part of the water macrofauna collection of
the Water Research Laboratory (Huamantinco and Ortiz, 2010).
Analysis of data
In order to evaluate the quality of the aquatic environment with
adequate efficiency, the surface water quality and the diversity of
taxa of benthic macroinvertebrate communities were determined.
To do this, multivariate statistical methods were used, such as mul-
tiple variance analysis (MANOVA), correlation analysis and cluster
analysis (Everitt et al., 2011).
Multiple variance analysis
To detect the difference between physical-chemical indicators
between wetlands, the generalized linear model was used by mul-
tiple variance analysis without interaction for electrical
conductivity-EC, biochemical oxygen demand-BOD5 and dissolved
total solids-DTS; and with interaction for the variables pH, chemi-
cal oxygen demand-COD, dissolved oxygen-DO, temperature,
nitrates and total phosphorus. The model was decided according
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
88.89% of the total phylum taxa. The greatest number of individu-
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).
The highest average value of abundance (120.30 ± 21.30) was
recorded in the Tragadero wetland where specimens of the Chi-
ronomidae family predominated, followed by Pomacocha and Cun-
cancocha (116.00 ± 21.76 and 59.50 ± 23.20, respectively) during
the dry season. The highest taxa richness (7.71 ± 1.80) was
recorded in the Pomacocha wetland and the highest dominance
(0.54 ± 0.07) in the Tragadero wetland. The diversity indices of
Simpson (1-D) and Shannon-Wiener (H ’) were higher in the Poma-
cocha wetland (0.74 ± 0.09, 1.57 ± 0.28, respectively) in the rainy
season. Similar behavior presented the mean values of Margalef
(1.41 ± 0.29) and Equitability (J) (0.84 ± 0.05), in this sampling
period.
Fig. 2 shows the grouping by similarity of the high Andean wet-
lands evaluated by indicators of biodiversity of benthic macroin-
vertebrates, in which it can be seen that wetlands are separated
by increasing the abundance of indicator specimens from dis-
turbed aquatic environments, especially where there is high avail-
ability of organic matter. The wetlands that presented greater
similarity were Pomacocha with Cuncancocha and Tragadero with
Incacocha. While the Ñahuinpuquio wetland is separated from the
rest of the wetlands, but conglomerates with the Incacocha and
Tragadero wetlands, revealing the low values presented by the
benthic macroinvertebrate diversity indices.
Relationships of the physical-chemical and bacteriological indicators
with the diversity of benthic macroinvertebrates of high Andean
wetlands
Table 4 shows the results of the multiple linear correlation anal-
ysis, using the Pearson coefficient for each pair of variables. It is
observed that the correlation of the variables temperature and
total dissolved solids with the abundance of benthic macroinverte-
brates are positive and highly significant (p < 0.01), while between
nitrates and abundance the correlation is negative and significant
(p < 0.05). Similar behavior of COD, total phosphorus and nitrates,
when correlated with richness, show negative and high signifi-
cance (p < 0.01); and pH, conductivity, BOD5 and thermotolerant
coliforms, when correlated with richness, are negative and signifi-
cant. The correlation of COD, BOD5, total phosphorus and thermo-
tolerant coliforms with the dominance of macroinvertebrates was
positive and highly significant, while the correlation of conductiv-
ity and total dissolved solids with dominance was positive and that
of dissolved oxygen with the dominance was negative, but signifi-
cant. Also, COD and BOD5 and total phosphorus showed highly sig-
nificant correlations with the Margalef index. The correlation of
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

Fig. 2. Grouping by similarity of high Andean wetlands evaluated by indicators of
biodiversity of benthic macroinvertebrates.
the Equitability (J) of benthic macroinvertebrate communities was
highly significant.
Discussion
Physico-chemical and bacteriological quality of water
The demand for water for its different uses is increasing rapidly
in recent decades, exerting strong pressure on the availability of
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
factor that would be contributing to the pH variation of the water
would be the photosynthetic activity that occurs during the day
(Craft et al., 2017). The highest values of conductivity recorded
during the dry season in the Tragadero wetland would be due to
the presence of ions and anions that are concentrated due to evap-
oration and the processes of degradation of organic matter that
accelerate the concentration of ions in the water (Effendi, 2016).
The dissolved oxygen together with the temperature determine
the richness and distribution patterns of benthic macroinverte-
brate families (Lake et al., 2017). According to MINEN (2015), the
conservation of the aquatic environment of wetlands classified in
category 2 of the environmental quality standards for water should
not have values of DO < 5 mg/L. However, the slightly low concen-
trations of DO recorded in the high Andean wetlands assessed dur-
ing the rainy and low water periods would be related to the
anthropogenic activities that take place in these ecosystems, such
as the intensive cultivation of Oncorhynchus mykiss, the entry of
cattle to graze and domestic activities such as washing clothes
and bathing of local people. These activities could be a source of
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
richness and distribution of aquatic biota (Seiler et al., 2015). The
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-
encing the water temperature. Phosphorus is one of the limiting
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
obtained from total phosphorus in the evaluated wetlands exceed
the EQS (0.035 mg/L). In addition, these high phosphorus concen-
trations reveal the contamination events through which the wet-
land crosses due to the development of anthropogenic activities;
among them the cattle activities, since the feces of the cattle are
a potential source of phosphorus.
Patterns of abundance, richness and diversity of benthic
macroinvertebrates
The results obtained show that the most abundant benthic
macroinvertebrates correspond to individuals of the class Insecta,
order Diptera. They also reveal differences between the communi-
ties of the five wetlands, with the Chironomidae family being the
most representative with a wide range in all zoogeographic regions
(Vamosi et al., 2012). The abundance recorded in the Cuncancocha
wetland during the rainy season confirms the average level of oxy-
genation of water bodies. Likewise, the greater abundance of these
individuals registered in the Tragadero wetland confirms the low
level of oxygenation of their waters. These results coincide with
those recorded in other studies in aquatic environments with
low oxygen levels, with dominance of Chironomidae and decrease
in macroinvertebrate density (Riens et al., 2013). However, these
effects are related to the decrease in water and food quality, as well
as to the interference of breathing mechanisms and other morpho-
physiological characteristics (Miserendino et al., 2012). Other fam-
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
Andean wetlands are Baetidae and Psychodidae, which are charac-
terized by living in oligotrophic waters.
The highest abundance of individuals of the order Ephe-
meroptera was recorded in the Pomacocha wetland in both sam-
pling seasons. These results reveal that the great majority of
species of this order have low tolerance to contamination
(Serrano Balderas et al., 2016). The Trichoptera order is an impor-
tant component of benthic communities and the basis of the
trophic chain of aquatic ecosystems. The greatest abundance of
the order Trichoptera was recorded in the Pomacocha wetland,
where the quality of the water is good. The most representative
family for its abundance is Leptophlebiidae. These results are cor-
roborated by Mereta et al. (2012), who point out that Trichoptera
are restricted to environments with vegetation, water depth and
conductivity. The order Coleoptera is the taxon that has colonized
all aquatic environments evaluated.
This study shows the positive and negative correlation,
significant and highly significant between the physical-chemical
indicators and the indicators of diversity of benthic macroinverte-
brates. These results coincide with those of Verdonschot et al.
(2012) and Mykrä et al. (2012), who refer that in areas with a
temperate climate, seasonality plays a very important role in the
structure of macroinvertebrate communities.
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,
according to the Margalef index, despite being higher than the
other gaps in study. Finally, the analysis of the results reveals the
significant and highly significant relationship of the physicochem-
ical factors with the diversity of benthic macroinvertebrates in the
five high Andean wetlands. However, the highly significant rela-
tionship of COD, BOD5 and total phosphorus with indicators of
diversity of these organisms reveals the strong anthropogenic pres-
sure that high Andean wetlands have been supporting.
Conclusions
Wetlands are fragile ecosystems and require protection from
continued development. The results obtained suggest the strong
influence of anthropogenic activities on the quality of the aquatic
environment and the diversity of benthic macroinvertebrates.
Although the values of pH, electrical conductivity, DO, nitrates
and thermotolerant coliforms of the wetlands under study are
within the range of the environmental quality standards for water
from lakes and lagoons in Peru, category 4, intended for the
conservation of the aquatic environment. The recorded COD and
BOD5 values exceeded these standards. The Tragadero wetland
has the greatest impact, with high values of temperature, TDS
and total phosphorus exceeding the standards that include these
ecosystems.
The communities of registered benthic macroinvertebrates var-
ied not only as a result of environmental variables and the spatial-
temporal pattern, but also because of the pressures exerted by
anthropogenic activities occurring in the wetlands under assess-
ment. Fourteen families of benthic macroinvertebrates were iden-
tified in five high Andean wetlands, with the Arthropoda phylum
being the most representative in abundance, richness and diver-
sity. The greatest abundance and dominance was recorded in the
Tragadero wetland and the greatest richness, diversity and
equitability of taxa was recorded in the Pomacocha wetland. In
addition, as a result of similarity grouping analysis, wetlands are
separated into two groups as the abundance of indicator specimens
of disturbed aquatic environments increases, especially where
there is high organic matter availability.
201
Conflict of interest
The authors declare that they have no conflict of interest.
Acknowledgements
The authors express our gratitude to the General Research Insti-
tute of the National University of Central Peru for the financing of
the study, to the Water Research Laboratory for allowing us to
make use of the equipment and materials for this study.
Author contributions
María Custodio developed the concept and design of the field
study and wrote the manuscript. She conducted analyses of ben-
thic macroinvertebrate and thermotolerant coliform communities,
provided interpretation of the data and verified laboratory data-
base. Fernán Chanamé carried out the determination of physical-
chemical parameters in situ and laboratory, Samuel Pizarro carried
out sediment sampling, compiled the data and elaborated the loca-
tion map of the wetlands under study, and Danny Cruz carried out
the statistical analysis and drafting of the results section. All
authors approved the final version before submission.
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