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Advanced Studies in Biology, Vol. 8, 2016, no. 4, 151 - 171 HIKARI Ltd, www.m-hikari.com http://dx.doi.org/10.12988/asb.2016.6830 How Water Quality in the Kabul River, Pakistan, Can be Determined with Algal Bio-indication Sophia Barinova 1 *, Izaz Khuram 2 , Asadullah 2 , Nadeem Ahmad 2 , Samin Jan 3 and Dong Hyun Shin 4 1 Institute of Evolution, University of Haifa, Mount Carmel 199 Abba Khoushi Ave., Haifa 3498838, Israel * Corresponding author 2 Department of Botany, University of Peshawar, Khyber, Pakhtunkhwa, Pakistan 3 Department of Botany, Islamia College Peshawar Khyber, Pakhtunkhwa Pakistan 4 School of Applied Biosciences, College of Agriculture and Life Sciences Kyungpook National University, Daegu 702-701, Republic of Korea Copyright © 2016 Sophia Barinova et al. This article is distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Abstract Altogether 209 species of algae and cyanobacteria has been revealed in 2014-2015 from four sites in the Kabul River that flow across the Peshawar Valley. Green algae, diatoms, and Charophyta filamentous algae were diverse and characterize regional feature in the river basin with high agricultural activity. Species richness and algal abundance were increase down the river. Index saprobity S varied between 1.55 and 1.59 (Class III of water quality) and reflects decreasing of water quality down the river as a result of pollutants impact, which brings mostly the Swat tributary. Bio-indication results show prevalence of benthic or plankto-benthic species, temperate temperature indicators, slow streaming middle oxygenated waters inhabitants, salinity-indifferents, eurysaprobes, mesotrophes, and autotrophic algae with tolerance to middle concentration of Nitrates that reflects middle polluted waters III-IV Class of Water

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Page 1: How Water Quality in the Kabul River, Pakistan, Can be ... Water Quality in the Kabul River, Pakistan, Can be Determined with Algal Bio-indication Sophia Barinova1*, Izaz Khuram 2,

Advanced Studies in Biology, Vol. 8, 2016, no. 4, 151 - 171

HIKARI Ltd, www.m-hikari.com http://dx.doi.org/10.12988/asb.2016.6830

How Water Quality in the Kabul River,

Pakistan, Can be Determined with Algal

Bio-indication

Sophia Barinova1*, Izaz Khuram2, Asadullah2, Nadeem Ahmad2,

Samin Jan3 and Dong Hyun Shin4

1Institute of Evolution, University of Haifa, Mount Carmel

199 Abba Khoushi Ave., Haifa 3498838, Israel *Corresponding author

2Department of Botany, University of Peshawar, Khyber, Pakhtunkhwa, Pakistan

3Department of Botany, Islamia College Peshawar

Khyber, Pakhtunkhwa Pakistan

4School of Applied Biosciences, College of Agriculture and Life Sciences

Kyungpook National University, Daegu 702-701, Republic of Korea

Copyright © 2016 Sophia Barinova et al. This article is distributed under the Creative

Commons Attribution License, which permits unrestricted use, distribution, and reproduction in

any medium, provided the original work is properly cited.

Abstract

Altogether 209 species of algae and cyanobacteria has been revealed in

2014-2015 from four sites in the Kabul River that flow across the Peshawar

Valley. Green algae, diatoms, and Charophyta filamentous algae were diverse and

characterize regional feature in the river basin with high agricultural activity.

Species richness and algal abundance were increase down the river. Index

saprobity S varied between 1.55 and 1.59 (Class III of water quality) and reflects

decreasing of water quality down the river as a result of pollutants impact, which

brings mostly the Swat tributary. Bio-indication results show prevalence of

benthic or plankto-benthic species, temperate temperature indicators, slow

streaming middle oxygenated waters inhabitants, salinity-indifferents,

eurysaprobes, mesotrophes, and autotrophic algae with tolerance to middle concentration of Nitrates that reflects middle polluted waters III-IV Class of Water

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152 Sophia Barinova et al.

Quality in the Kabul River. Our analysis shows that integral bio-indication in

water quality assessment with using of algal communities can give relevant results

of self-purification possibility, which can be employed in purpose of monitoring

the regional water quality as economy and resultative method.

Keywords: Periphyton, Phytoplankton, River, Water Quality, Bio-indication

1 Introduction

The ongoing climate change can be taken into account in addition to the

human factor. The global warming primarily influences the hydrological regime

of water ecosystems in arid regions [1] such as of Pakistan.

Algal diversity ecologically plays an important role in the understanding of

aquatic ecosystem, their productivity and water quality [2]. Habitat characteristics

play an important role to affect freshwater algal communities [3]. The study of

algae at their habitats is the prime object of algal ecology [4]. Rivers are complex

ecosystems consisting of biotic communities (biocoenoses) and diverse habitats

(biotopes). The characteristics of the habitats change from the head-waters to the

sites of eventual discharge [5].

It is known that the pollution of the river due to the number of people on its

banks and the intensity of development of the economy and have synergetic effect

with global warming. Because studies of the Kabul River in the early stages, there

is no published information on the anthropogenic load of the studied section of the

river, so we used only the impressions in the process of collecting.

The aquatic objects in Pakistan are represented mostly the rivers. Algal

diversity of the Pakistan rivers can help in ecological assessment of the water

quality and water using intensity for agriculture. The algal communities in

Pakistan rivers start to study in last two decades and is so far from exhaustive.

Algal flora of the Kunhar River, Pakistan, was ecologically studied for the first

time [6]. Algal Diversity of the Meenachil River, India was studied during the

premonsoon and monsoon period of 2014 [7]. Systematics and geographic

distribution of Chroococcus was studied in Pakistan [8]. Algal species diversity

distribution and its relationships to altitude of aquatic habitats were studied on the

Hindu Cush Mountains communities of the Swat River [9]. The importance of

water resources quality in Pakistan is now one of major problem. Therefore, the

state try to find some economy methods for dissolve this problem. One of the

methods for water resources quality assessment is the bio-indication. Algal

bio-indication approaches were employed in Pakistan earlier for the Swat River

algal communities [9]. The Swat River is the upper high mountain tributary of the

Kabul River. In the Kabul River were no more publications about algal diversity

than about freshwater green algal biofouling of boats [10].

The aim of present study was to reveal algal diversity in the Kabul River sites

before and after the Swat River input and employ the bio-indication methods for

the water quality assessment.

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How water quality in the Kabul River, Pakistan… 153

Description of study site

Peshawar Valley is the most distinct region within the entire Khyber

Pakhtunkhwa, Pakistan. The Valley lies on the coordinates about 34°07’58’’ N

and 71°41’45’’E and has an altitude of about 335 m [11].

The climate of Peshawar Valley has been termed as a modified

Mediterranean type of climate. The summers are hot and the winters are cold. The

range of temperature varies between 50C° (highest) to -3C° (lowest). Four

seasons are recognized in Peshawar valley [11, 12].

The Kabul River is an itinerary between Afghanistan and Pakistan. It is 700

km long, of which 563.27 km is in Afghanistan and 136.79 km in Pakistan [13]. It

is rising in North Eastern Afghanistan at the base of the Wonay Pass in the

Paghman Range (Selsela-e-Kuh-e-Paghman) and ends in the Indus River near

Khairabad, North-West of Islamabad, Pakistan [12]. The depth and width of the

channel ratio is highly flexible in different seasons and vary in 2-3 m deep and

30-90 m width. The average discharge at Warsak Dam is 20.5×103m3sec−1. The

variations in river flow are the result of seasonal rains, glacial and snowmelt [14].

The major tributary is the Swat River, originating in Kalam travels in the hills

of Swat Valley and enters to the Kabul River near Jalabella. Two other tributaries

are the Bara River and the Jindai River, which flow into the Kabul River near

Khairabad [12]. Four research sites were selected in the Peshawar Valley (Figure

1) to assess the algal diversity, ecology, and water quality in the Kabul River:

Warsak (1), Sardaryab (2), Nowshera (3) and Khairabad (4).

Figure 1. Peshawar Valley with the Kabul River sampling sites

2 Materials and Methods

1. Field sampling

Sampling was carried out during the autumn and spring seasons in 2014-2015.

A total of 30 samples were collected from four sampling sites in a 100-meter

radius on each individual location from different habitats including phytoplankton

and periphyton (epiphyton, epilithon, and epipsammon). The samples were trans-

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154 Sophia Barinova et al.

ported into the Phycology and Tissue Culture laboratory, Department of Botany,

University of Peshawar, in standard specimen bottles with icebox.

2. Preservation, Labeling and Storage

Temporary preservation was processed immediately after sampling with

neutral Lugol’s Iodine solution, 0.5 ml per 100 ml water sample, and stored for a

short time [15].

Permanent preservation of samples was in 3 % FAA (Formalin, acetic acid and

alcohol) and kept for a long time to avoid spoilage [15]. The permanently

preserved specimens were vouchered and submitted to the Department of Botany

herbarium, University of Peshawar.

3. Laboratory Processing

Microscopic morphology of the Non-Diatomaceous isolates was determined

by using the wet-mount staining method [15]. This was done by using a sterile

micromanipulator to pick up algal filaments from temporarily preserved samples

and placed onto a clean glass slide on which a drop of distilled water had been

added. A drop of lactophenol cotton blue stain was added, and the preparation was

covered with clean cover slips. The slides were subsequently viewed under 10×,

20×, 40× 60× and 100× Nikon Eclipse E200 microscope objectives. Images of the

taxa were taken with a BRESSER digital microscope. The Diatomaceous isolates

were cleaned by using peroxide (H2O2) technique [16] (Swift, 1967). The empty

frustules were then mounted and analyzed for their morphology. Standard

references [2,17-23] were usede for taxonomic identification.

Physicochemical properties of the water from the sampling sites were

measured in parallel with algal sampling. Temperature and water pH were

measured with HANNA HI98190 portable meter and Turbidity with HANNA

HI98703 meter in the laboratory. Electrical conductivity and Total Dissolved

Solids (TDS) of the water samples were measured with HANNA HI98192 meter

in the laboratory. Total Suspended Solids (TSS) values in the water samples were

measured with HACH TSS meter in the laboratory. Dissolved oxygen (DO) and

Biochemical Oxygen Demand (B.O.D.) were measured by using HANNA

HI98193 meter in the laboratory.

Alkalinity as CaCO3 was analyzed by titration against standard sulphuric acid.

Hardness as CaCO3 and Sulphates were analyzed by complexometric titrations

using EDTA (0.01M). Nitrites and Nitrates were analyzed by spectrophotometric

(Colorimetric) method. Ammonia and Phosphates (PO43-) were analyzed by

spectrophotometric method using Nessler’s reagent. Phosphates (PO43-) Chlorides

(Cl-) were determined by titrating against silver nitrate (0.1 N) using potassium

chromate as indicator.

Ecological preferences of revealed algal species were assessed according [24].

Bio-indication approaches were taken from these references and later [25].

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How water quality in the Kabul River, Pakistan… 155

Indices saprobity S [26, 27] were calculated on the basis of identified species

for each community and quantitative investigations of phytoplankton as:

𝑆 = ∑ (𝑠𝑖 × 𝑎𝑖) ∑(𝑎𝑖)

𝑛

𝑖=1

𝑛

𝑖=1

(Eq. 1)

Where: S – Saprobity index of algal community; si – species–specific saprobity

index; ai – species abundance.

The integral index of aquatic ecosystem sustainability (WESI) was

constructed on results of our studies [24, 25]. Indices calculation is based on the

water quality ranks as determined by Sládeček’s saprobity indices and nitrate (or

phosphates) concentrations rank.

WESI = Rank S / Rank N-NO3 (Eq. 2)

where:

Rank S – the rank of water quality according to the range of the Sládeček’s

saprobity indices calculated for the sampling station.

Rank N-NO3 – water quality rank according to the range of nitric-nitrogen

concentrations scale.

At WESI ≥ 1, the photosynthetic level is positively correlated with the level of

nitrate concentration. At WESI < 1, photosynthesis is suppressed (presumably due

to a toxic disturbance).

2 Results and Discussion

1. Chemical variables

The water variables dynamic over sampling stations of the Kabul River are

represented in Figure 2. It shown that water temperature, pH, conductivity, TDS,

TSS, Salinity, Chlorides, and Alkalinity were increased down the river.

Concentration of Nitrates, Nitrites, and Ammonia were dramatically increased

immediately after the Swat River tributary input in site 2. In the same time the

Dissolved oxygen, Total Hardness, and Sulfates were decreased in site 2 whereas

the Phosphates here increased. That all let us to conclude that the Swat tributary

influence on the water quality of the Kabul River is high because its water was

slightly low enriched by major ions but bring more polluted waters to the Kabul

River. Hydrochemical variables of the Kabul River in autumn 2014 and spring

2015 are corresponded to the levels of middle polluted water, with increasing of

the organic pollution as BOD down the river. Index Saprobity S, calculated with

species abundance, is increased after station 2 in sites Nowshera and Khairabad

from 1.55 up to 1.59. Index reflects middle polluted water Class III of water quality

with developed community (Figure 3). It is known that temperature, phosphorus

and nitrogen are essential elements for controlling the development of algae

[28-31]. Therefore, our analysis reveals the trophic base for algal community

development, which increased down the river. This situation looks like similar to

it in the Songhua River from climatically similar region of China [32] where water variables of pollution also increased down the river with index saprobity S

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156 Sophia Barinova et al.

in the same range 1.57-1.79 that reflect Class III of water quality.

Figure 2. Dynamic of major chemical variables over the Kabul River sampling

stations

2. Algal communities

Altogether 209 species of algae and cyanobacteria were found in four sites of

the Kabul River (Table 1). In Figure 3 are presented qualitative (No of Species)

and quantitative (Abundance Scores) data for four sites. Species richness and algal

abundance are increased similar down the river (Figure 4). Whereas major

abundance in communities was represents by charophytes (Figure 3), species

richness was mostly represented by charophyta also (Figure 4). The algal

community in the major left high mountain tributary of the Kabul River the Swat

River was not so reach in species and strongly regulated by water temperature [9].

Nevertheless, the community structure in the Swat River which flow below 1400

m was similar to it in the studied part of the Kabul River with prevalence of green

algae and diatoms. It is remarkable that Charophyta algae represent about a

quarter of the algal flora in the both rivers and the most diverse of all was

Spirogyra and other filamentous algae. It can be represent some regional feature

in the river basin with high agricultural activity. The prevalence of green algae in

the riverine community is relater also with the latitude of the river basin and

therefore with sunlight intensity such as in the rivers Ukraine [33], China [32],

and Israel [25, 34].

Figure 3. Dynamic of major biological variables over the Kabul River sampling

stations

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How water quality in the Kabul River, Pakistan… 157

Table 1. Ecological preferences of algal species and its abundance over the sites in

the Kabul River

Taxa W S N K Hab T Oxy Sal Wat Sap Index

S Tro Nutr

Cyanobacteria

Aphanocapsa incerta (Lemmermann)

G.Cronberg & Komárek 5 5 5 5 P-B - - i - b 2.2 me -

Chroococcus minimus (Keissler)

Lemmermann 1 1 1 1 P-B - - hl - - - o-m -

Chroococcus turgidus (Kützing)

Nägeli 1 1 1 1 P-B,S - aer hl - x-b 0.8 - -

Gloeocapsa punctata Nägeli 5 5 5 5 Ep,S - aer hl - - - - -

Gloeocapsa rupestris Kützing 5 5 0 5 Ep,S - aer - - - - - -

Kamptonema formosum (Bory ex

Gomont) Strunecký, Komárek &

J.Smarda

0 0 3 3 P-B,S - st - - a 3.1 me -

Lyngbya aestuarii Liebman ex

Gomont 0 1 2 0 P-B,S - - mh - o 1.3 - -

Lyngbya majuscula Harvey ex

Gomont 0 2 2 2 - - - - - - - - -

Lyngbya martensiana Meneghini ex

Gomont 2 2 0 0 P-B,S warm st-str - - b-o 1.7 o-m -

Merismopedia convoluta Brébisson

ex Kützing 5 0 0 0 P-B - - - - b-a 2.5 o-m -

Merismopedia tenuissima

Lemmermann 5 5 5 5 P-B - - hl - b-a 2.4 e -

Merismopedia chondroidea Wittrock 0 5 5 5 - - - - - - - - -

Merismopedia trolleri Bachmann 1 2 2 2 - - - - - - - - -

Microcoleus autumnalis (Gomont)

Strunecky, Komárek & J.R.Johansen 0 0 0 5 B,S - st-str - - b 2.3 - -

Microcoleus setchellianus (Gomont)

Strunecky, Komárek & Johansen 3 3 3 3 - - - - - - - - -

Microcystis aeruginosa (Kützing)

Kützing 3 3 0 0 P - - hl - b 2.1 e -

Oscillatoria anguina Bory ex Gomont 5 5 5 5 B,S - - - - - - o-m -

Oscillatoria limosa C.Agardh ex

Gomont 0 0 0 1 P-B - st-str hl - a-o 2.6 e -

Oscillatoria major Vaucher ex Forti 0 0 1 2 B,Ep - - - - b 2.3 m -

Oscillatoria princeps Vaucher ex

Gomont 1 2 2 2 P-B,S - st-str - - a-o 2.8 o-m -

Oscillatoria tenuis C.Agardh ex

Gomont 0 1 0 1 P-B,S - st-str hl - a-o 2.6 me -

Oscillatoria jenensis G.Schmid 0 0 2 2 - - - - - - - - -

Phormidium ambiguum Gomont 3 3 3 3 B,S eterm st-str i - b 2.3 me -

Phormidium articulatum

(N.L.Gardner) Anagnostidis &

Komárek

3 3 3 3 - - - - - - - - -

Phormidium breve (Kützing ex

Gomont) Anagnostidis & Komárek 3 3 0 3 P-B,S - st,aer - - a 3.1 - -

Phormidium chalybeum (Mertens ex

Gomont) Anagnostidis & Komárek 3 3 3 3 P-B,S - st-str - - a 3.3 e -

Phormidium incrustatum Gomont ex

Gomont 3 3 3 3 B - st-str - - x 0.1 o -

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158 Sophia Barinova et al.

Table 1. (Continued): Ecological preferences of algal species and its abundance

over the sites in the Kabul River

Phormidium irriguum (Kützing ex

Gomont) Anagnostidis & Komárek 3 3 3 3 B,Ep - aer - - - - me -

Phormidium lucidum Kützing ex

Gomont 0 3 3 3 P-B warm st-str hl - - - - -

Phormidium nigrum (Vaucher ex

Gomont) Anagnostidis & Komárek 1 0 1 0 P-B warm - - - b 2.2 m -

Phormidium retzii Kützing ex

Gomont 0 3 3 3 B,S - st-str - - o-b 1.4 o -

Phormidium stagninum Anagnostidis 1 1 2 1 B,Ep - - - - - - o-m -

Phormidium subfuscum Kützing ex

Gomont 3 3 3 3 B,S - st-str - - o-b 1.5 o -

Phormidium uncinatum Gomont ex

Gomont 0 0 3 3 P-B,S eterm st-str i - b 2.3 me -

Phormidium nigroviride (Thwaites ex

Gomont) Anagnostidis & Komárek 0 3 3 3 - - - - - - - - -

Spirulina major Kützing ex Gomont 0 0 1 1 P-B,S warm st hl - a 3.4 - -

Spirulina nordstedtii Gomont 0 1 1 1 B - - mh - - - - -

Bacillariophyta

Achnanthes elata

(Leuduger-Fortmorel) H.P.Gandhi 0 2 2 2 - - - - - - - - -

Aulacoseira granulata (Ehrenberg)

Simonsen 1 1 1 1 P-B temp st-str i es b 2.0 me ate

Cocconeis placentula Ehrenberg 3 3 3 0 P-B temp st-str i es o 1.35 me ate

Cyclotella meneghiniana Kützing 1 1 0 1 P-B temp st hl sp a-o 2.8 e hne

Cymatopleura solea (Brébisson) W.

Smith 2 0 0 0 B - st-str i - b 2.1 e ate

Cymbella affinis Kützing 3 3 3 3 B temp st-str i sx o 1.1 ot ats

Cymbella cistula (Ehrenberg)

O.Kirchner 0 0 0 3 B - st-str i sx o 1.2 e ats

Cymbella tumida (Brébisson) van

Heurck 2 2 1 2 B temp str i sx b 2.2 me ats

Diatoma tenuis C.Agardh 2 3 3 3 P-B - st-str hl sx o 1.3 e ate

Diatoma vulgaris Bory 3 3 0 3 P-B - st-str i sx b 2.2 me ate

Didymosphenia geminata (Lyngbye)

Mart.Schmidt 1 1 1 1 B - st-str i sx o-x 0.7 ot -

Fragilaria capucina Desmazières var.

capucina 0 2 2 0 P-B - - i es b-o 1.6 m -

Fragilaria capucina var. vaucheriae

(Kützing) Lange-Bertalot 2 3 3 1 P-B,Ep - st-str i sx o-a 1.95 e ate

Fragilaria crotonensis Kitton 0 0 2 1 P - st-str I es o-b 1.5 m ate

Fragilaria goulardii (Brébisson ex

Grunow) Lange-Bertalot 0 0 1 2 - - - - - - - - -

Frustulia vulgaris (Thwaites) De Toni 1 0 1 0 P-B - st i es o-a 1.8 me ate

Gomphonema acuminatum Ehrenberg 2 2 2 3 B - st i es o-b 1.4 o-m ats

Gomphonema augur Ehrenberg 0 2 3 2 B - str i es o-b 1.5 me ats

Gomphonema micropus Kützing 1 2 0 0 B - str i es o 1.3 ot ate

Gyrosigma acuminatum (Kützing)

Rabenhorst 1 1 1 1 B cool st-str i es o-a 1.95 me ate

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How water quality in the Kabul River, Pakistan… 159

Table 1. (Continued): Ecological preferences of algal species and its abundance

over the sites in the Kabul River

Gyrosigma nodiferum (Grunow)

Reimer 0 0 1 2 B - - i es b-o 1.7 - -

Mastogloia elliptica (C.Agardh)

Cleve 0 0 2 1 B - - mh - - - - -

Melosira crenulata (Ehrenberg)

Kützing 0 1 2 0 P-B - - - - x-o 0.5 - -

Melosira varians C.Agardh 0 0 2 2 P-B temp st-str hl es b 2.1 me hne

Meridion circulare (Greville)

C.Agardh 2 0 0 0 B - str i es o 1.1 o-m ate

Navicula radiosa Kützing 2 2 1 3 P-B temp st-str i es o 1.3 me ate

Navicula tripunctata (O.F.Müller)

Bory 0 3 2 3 P-B - st-str i es b-o 1.7 e ate

Nitzschia amphibia Grunow 0 0 0 2 P-B,S temp st-str i sp b 2.1 e hne

Nitzschia intermedia Hantzsch 0 1 1 2 P-B - - i es b 2.0 e -

Nitzschia palea (Kützing) W.Smith 2 1 2 2 P-B temp - i sp a-o 2.8 he hce

Nitzschia paleacea Grunow 3 2 2 1 P-B - st-str i es b 2.2 e hce

Nitzschia solita Hustedt 1 1 2 1 B - st mh es a-b 3.6 e -

Nitzschia vitrea G.Norman 0 1 1 1 P-B - - mh - a-o 2.7 e -

Pinnularia viridis (Nitzsch)

Ehrenberg 2 1 2 2 P-B temp st-str i es x 0.3 o-e ate

Rhoicosphenia abbreviata

(C.Agardh) Lange-Bertalot 0 1 2 1 B - st-str i es o-a 1.9 me ate

Rhopalodia gibba (Ehrenberg) Otto

Müller 0 2 1 0 B temp - i es o-b 1.4 o-m -

Stenopterobia pelagica Hustedt 1 2 1 1 - - - - - - - - -

Stephanodiscus hantzschii Grunow 0 1 2 1 P temp st i es a-o 2.7 o-m hne

Surirella ovalis Brébisson 0 0 0 1 P-B - st-str I es a 3.0 me ate

Surirella robusta Ehrenberg 1 1 1 1 P-B - st-str I es x-o 0.5 ot -

Surirella splendida (Ehrenberg)

Kützing 1 1 1 1 P-B - st-str i - o-x 0.7 me -

Surirella striatula Turpin 0 1 1 0 P-B temp - hl - b 2.0 e -

Synedra cyclopum Brutschy 2 2 3 3 B - - i - o-b 1.5 ot -

Tryblionella compressa (J.W.Bailey)

M.Poulin 2 2 2 2 B eterm - mh - - - - -

Ulnaria ulna (Nitzsch) Compère 2 1 1 1 P-B temp st-str i es b-a 2.4 o-e ate

Xanthophyta

Tribonema affine (Kützing) G.S.West 5 5 5 5 B - - hb - x-b 0.8 - -

Tribonema microchloron Ettl 0 0 5 5 - - - - - - - - -

Tribonema minus (Wille) Hazen 0 0 5 5 B - - i - x-b 0.9 - -

Tribonema viride Pascher 5 5 5 5 P-B - - i - o-x 0.7 - -

Tribonema delicatissimum Ettl 0 0 0 5 - - - - - - - - -

Vaucheria fontinalis (Linnaeus)

T.A.Christensen 5 5 5 5 B - - - - o 1.2 - -

Vaucheria sessilis (Vaucher) De

Candolle 5 5 0 0 B - - - - o-b 1.5 - -

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160 Sophia Barinova et al.

Table 1. (Continued): Ecological preferences of algal species and its abundance

over the sites in the Kabul River

Vaucheria undulata C.-C.Jao 5 0 5 0 - - - - - - - - -

Vaucheria longipes Collins 0 5 5 5 - - - - - - - - -

Euglenophyta

Euglena mutabilis F.Schmitz 0 2 0 1 B - st-str - - x-b 0.8 - -

Euglena pisciformis Klebs 1 1 1 1 P-B eterm st-str mh - a 3.0 - -

Euglena sanguinea Ehrenberg 2 1 1 1 P-B - st-str i - o 1.25 - -

Euglena viridis (O.F.Müller)

Ehrenberg 0 1 1 0 P-B,S eterm st-str mh - i 4.0 - -

Phacus acuminatus Stokes 1 1 1 1 P-B eterm st-str i - b-a 2.5 - -

Phacus caudatus Hübner 0 1 1 1 P-B eterm st-str i - b 2.3 - -

Chlorophyta

Chaetophora elegans (Roth)

C.Agardh 4 4 4 4 B - - - - o 1.2 - -

Chaetophora lobata Schrank 4 4 4 4 B - - - - o 1.1 - -

Chlamydomonas debaryana

Gorozhankin 0 1 2 1 P - - - - a 3.0 - -

Chlamydomonas ehrenbergii

Gorozhankin 0 2 0 2 P - - - - p-a 3.5 - -

Chlamydomonas globosa J.W.Snow 0 0 0 1 P,S - - - - o-a 1.9 - -

Chlorella minutissima Fott &

Nováková 0 2 3 0 - - - - - - - - -

Chlorella vulgaris Beyerinck 0 0 3 3 P-B,pb,S - - hl - a 3.1 - -

Chlorococcum infusionum (Schrank)

Meneghini 1 1 2 2 P,S - st - - a-o 2.7 - -

Cladophora fracta (O.F.Müller ex

Vahl) Kützing 4 4 4 4 P-B - st-str - - b 2.3 - -

Cladophora glomerata (Linnaeus)

Kützing var. glomerata 4 4 4 4 P-B - st-str i - o-a 1.9 - -

Cladophora glomerata var. crassior

(C.Agardh) Hoek 4 4 4 4 B - - - - o-a 1.9 - -

Cladophora rivularis (Linnaeus)

Hoek 4 4 4 4 - - - - - - - - -

Dactylococcus infusionum Nägeli 0 4 4 4 - - - - - - - - -

Desmodesmus abundans (Kirchner)

E.Hegewald 0 1 1 2 P-B - st-str - - o-a 1.9 - -

Desmodesmus communis

(E.Hegewald) E.Hegewald 0 0 1 0 P-B - st-str i - b 2.15 - -

Hydrodictyon reticulatum (Linnaeus)

Bory 4 4 0 4 P-B - st - - o-a 1.8 - -

Microspora amoena (Kützing)

Rabenhorst 0 5 5 5 B - - - - x-b 0.8 - -

Microspora pachyderma (Wille)

Lagerheim 5 5 5 5 B - - - - o 1.0 - -

Microspora stagnorum (Kützing)

Lagerheim 0 0 0 5 B - st - - b-o 1.6 - -

Microspora willeana Lagerheim 5 5 5 5 B - - - - o 1.2 - -

Microspora wittrockii (Wille)

Lagerheim 0 5 5 5 - - - - - - - - -

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How water quality in the Kabul River, Pakistan… 161

Table 1. (Continued): Ecological preferences of algal species and its abundance

over the sites in the Kabul River Mychonastes homosphaera (Skuja)

Kalina & Puncochárová 0 1 1 0 P-B,S - st - - a 3.1 - -

Oedogonium capilliforme Kützing ex

Hirn 5 5 5 5 - - - - - - - - -

Oedogonium crassum Wittrock ex

Hirn 0 5 5 5 - - - - - - - - -

Oedogonium curvum Pringsheim ex

Hirn 0 5 5 5 - - - - - - - - -

Oedogonium echinospermum

A.Braun ex Hirn 0 5 5 5 B - - - - o 1.1 - -

Oedogonium gracilius Tiffany 5 5 5 5 - - - - - - - - -

Oedogonium itzigsohnii De Bary ex

Hirn 0 5 0 0 B - - - - o 1.1 - -

Oedogonium princeps Wittrock ex

Hirn 0 0 5 5 - - - - - - - - -

Pandorina morum (O.F.Müller) Bory 0 1 1 1 P - st i - b 2.3 - -

Rhizoclonium africanum Kützing 5 5 5 5 - - - - - - - - -

Rhizoclonium crassipellitum West &

G.S.West 5 5 5 5 - - - - - - - - -

Rhizoclonium hieroglyphicum

(C.Agardh) Kützing 5 5 5 5 B - st-str hl - o-a 1.9 - -

Rhizoclonium fontanum Kützing 5 5 5 5 - - - - - - - - -

Scenedesmus aculeotatus Reinsch 1 1 1 1 P-B - st-str - - b-o 1.6 - -

Scenedesmus armatus (Chodat)

Chodat 1 0 0 0 P-B - st-str - - b 2.2 - -

Stigeoclonium lubricum (Dillwyn)

Kützing 0 4 4 4 B - - - - b 2.3 - -

Stigeoclonium subsecundum

(Kützing) Kützing 4 4 4 4 B - - - - b 2.3 - -

Tetraëdron caudatum (Corda)

Hansgirg 1 1 2 1 P-B - st-str i - b 2.0 - -

Tetraëdron minimum (A.Braun)

Hansgirg 2 1 1 1 P-B - st-str i - b 2.1 - -

Ulothrix aequalis Kützing 5 5 5 5 B - - - - o 1.3 - -

Ulothrix tenerrima (Kützing) Kützing 0 0 5 0 B - st i - o-a 1.8 - -

Ulothrix tenuissima Kützing 5 0 5 5 B - - i - b-o 1.6 - -

Ulothrix zonata (F.Weber & Mohr)

Kützing 0 5 0 5 P-B - st-str i - o-a 1.8 - -

Charophyta

Chara braunii var. schweinitzii

(A.Braun) Zaneveld 4 4 4 4 B - - - - o 1.2 - -

Chara vulgaris Linnaeus 4 4 4 4 B - st-str - - o 1.1 - -

Closterium acerosum Ehrenberg ex

Ralfs 1 1 1 0 P-B - st-str i - a-o 2.6 e -

Closterium attenuatum Ralfs 0 0 1 1 B - - - - - - m -

Closterium ehrenbergii Meneghini ex

Ralfs 0 1 1 1 P-B - st-str hb - o-b 1.5 me -

Closterium incurvum Brébisson 0 1 1 1 B - - - - o-a 1.8 me -

Closterium moniliferum Ehrenberg ex

Ralfs 2 1 1 1 P-B - st-str i - b 2.1 me -

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162 Sophia Barinova et al.

Table 1. (Continued): Ecological preferences of algal species and its abundance

over the sites in the Kabul River

Closterium parvulum Nägeli 0 1 0 0 P-B - - i - b 2.0 m -

Cosmarium angulosum Brébisson 1 1 1 1 B - - - - - - m -

Cosmarium bioculatum Brébisson ex

Ralfs 1 1 1 1 P-B - st-str hb - x-o 0.5 m -

Cosmarium crenatum Ralfs ex Ralfs 0 1 0 0 B,aer - aer - - - - m -

Cosmarium granatum Brébisson ex

Ralfs 1 0 0 1 B - st-str i - o 1.2 m -

Cosmarium impressulum Elfving 0 1 1 1 B,P-B - - hb - b-o 1.6 m -

Cosmarium laeve Rabenhorst 0 1 1 1 P-B - st-str hb - o-a 1.9 me -

Cosmarium punctatum Nordstedt 1 1 0 1 - - - - - - - - -

Cosmarium subcrenatum Hantzsch 2 1 1 1 B,aer - aer - - o 1.1 m -

Cosmarium subtumidum Nordstedt 0 0 2 2 B - - - - - - o-m -

Cosmarium turpinii Brébisson 1 1 1 2 P-B - - i - o-x 0.7 me -

Mougeotia americana Transeau 5 5 5 5 - - - - - - - - -

Mougeotia calcarea (Cleve) Wittrock 5 5 5 5 B - - - - o-x 0.7 - -

Mougeotia floridana Transeau 5 5 5 5 - - - - - - - - -

Mougeotia laevis (Kützing)

W.Archer 5 5 5 0 B - - - - o 1.0 - -

Mougeotia maltae Skuja 0 5 5 5 B - - - - o 1.0 - -

Mougeotia micropora Taft 0 0 0 5 - - - - - - - - -

Mougeotia nummuloides (Hassall) De

Toni 0 5 0 5 B - - - - o 1.0 - -

Mougeotia robusta (De Bary)

Wittrock 5 0 0 5 B - - - - o 1.0 - -

Mougeotia viridis (Kützing) Wittrock 5 5 5 0 B - - - - o 1.3 - -

Spirogyra australica Czurda 5 5 5 5 - - - - - - - - -

Spirogyra bellis (Hassall) P.Crouan &

H.Crouan 5 5 0 5 - - - - - - - - -

Spirogyra borgeana Transeau 5 5 5 5 - - - - - - - - -

Spirogyra californica Stancheva,

J.D.Hall, McCourt & Sheath 0 0 5 0 - - - - - - - - -

Spirogyra cataeniformis (Hassall)

Kützing 5 5 5 5 - - - - - - - - -

Spirogyra colligata Hodgetts 5 5 5 5 - - - - - - - - -

Spirogyra crassa (Kützing) Kützing 5 5 5 5 B - - - - o-b 1.5 - -

Spirogyra daedaleoides Czurda 5 5 5 5 - - - - - - - - -

Spirogyra elongata (Vaucher)

Dumortier 5 5 5 5 - - - - - - - - -

Spirogyra fluviatilis Hilse 5 5 5 5 P-B - - oh - x-b 0.8 - -

Spirogyra juliana Stancheva,

J.D.Hall, McCourt & Sheath 5 5 5 5 - - - - - - - - -

Spirogyra kuusamoensis Hirn 0 5 5 5 - - - - - - - - -

Spirogyra lutetiana Petit 5 0 0 0 - - - - - - - - -

Spirogyra majuscula Kützing 5 5 5 5 B - - - - o-a 1.8 - -

Spirogyra maxima (Hassall) Wittrock 5 5 5 5 B - - - - o 1.1 - -

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How water quality in the Kabul River, Pakistan… 163

Table 1. (Continued): Ecological preferences of algal species and its abundance

over the sites in the Kabul River

Spirogyra micropunctata Transeau 5 5 5 5 - - - - - - - - -

Spirogyra notabilis Taft 5 5 5 5 - - - - - - - - -

Spirogyra parvula (Transeau) Czurda 5 5 5 5 B - st-str - - - - - -

Spirogyra pratensis f. minor (Liu)

C.-C.Jao 5 5 5 5 - - - - - - - - -

Spirogyra protecta H.C.Wood 5 5 5 5 - - - - - - - - -

Spirogyra scrobiculata (Stockmayer)

Czurda 5 5 5 0 - - - - - - - - -

Spirogyra setiformis (Roth) Martens

ex Meneghini 0 5 5 5 - - - - - - - - -

Spirogyra spreeiana Rabenhorst 0 0 0 5 - - - - - - - - -

Spirogyra teodorescui Transeau 0 5 0 5 - - - - - - - - -

Spirogyra varians (Hassall) Kützing 5 5 5 5 P-B - - oh - b 2.1 - -

Spirogyra weberi Kützing var. weberi 5 5 5 5 - - - - - - - - -

Spirogyra weberi var. grevilleana

(Hassal) O.Kirchner 5 5 5 5 B - st - - - - - -

Spirogyra aequinoctialis G.S.West 5 5 5 5 - - - - - - - - -

Temnogyra collinsii I.F.Lewis 5 5 5 5 - - - - - - - - -

Zygnema aplanosporum Stancheva,

J.D.Hall & Sheath 5 5 5 5 - - - - - - - - -

Zygnema argillosum Kadlubowska 0 0 5 5 - - - - - - - - -

Zygnema carinthiacum

Beck-Mannagetta 5 5 5 5 B - - - - o 1.0 - -

Zygnema cruciatum (Vaucher)

C.Agardh 0 5 5 5 B - - - - x-b 0.8 - -

Zygnema cylindricum Transeau 5 5 5 5 - - - - - - - - -

Zygnema giganteum Randhawa 0 0 0 5 - - - - - - - - -

Zygnema inconspicuum Czurda 5 5 5 5 B - - - - o 1.0 - -

Zygnema maius Czurda 0 5 5 5 - - - - - - - - -

Zygnema normanii Taft 5 5 5 5 - - - - - - - - -

Zygnema stellinum (O.F.Müller)

C.Agardh 5 5 5 5 B - - - - o-x 0.7 - -

Zygnema sterile Transeau 5 5 5 5 B - - - - o 1.0 - -

Zygnemopsis transeauana Randhawa 0 5 5 5 - - - - - - - - -

Table legend: Sites: W – 1. Warsak; S – 2. Sardaryab; N – 3. Nowshera; K – 4. Khairabad. Substrate preferences (Habitat): P – planktonic,

P-B – plankto-benthic, B – benthic, Ep – epiphyte, S - soil. Temperature preferences (Temp): cool – cool-water, temp – temperate, eterm –

eurythermic, warm – warm-water. Oxygenation and streaming (Oxy): st – standing water, str – streaming water, st-str – low streaming

water, aer – aerophiles. Halobity degree according Hustedt [35] (Sal): hb – oligohalobes-halophobes, i – oligohalobes-indifferent, mh –

mesohalobes, hl – halophiles. Saprobity groups according Watanabe et al. [36] (D): sp – saprophiles, es – eurysaprobes, sx – saproxenes.

Species-specific Index of Saprobity (S). Self-purification zone preferences (Sap): x – xenosaprob; x-o – xeno-oligosaprob; o-x –

oligo-xenosaprob; x-b – xeno-beta-mesosaprob; o – oligosaprob; o-b – oligo-beta-msosaprob; b-o – beta-oligosaprob; o-a –

oligo-alpha-mesosaprob; b – beta-mesosaprob; b-a – beta-alpha-mesosaprob; a – alpha-mesosaprob; a-p – alpha-polysaprob; a-b –

alpha-beta-mesosaprob; i – i-eusaprob. Trophic state (Tro) [37]: ot – oligotraphentic; o-m – oligo-mesotraphentic; m – mesotraphentic; me –

meso-eutraphentic; e – eutraphentic; he – hypereutraphentic; o-e – oligo- to eutraphentic (hypereutraphentic). Nitrogen uptake metabolism

(Aut-Het) [37]: ats – nitrogen-autotrophic taxa, tolerating very small concentrations of organically bound nitrogen; ate –

nitrogen-autotrophic taxa, tolerating elevated concentrations of organically bound nitrogen; hne – facultatively nitrogen-heterotrophic taxa,

needing periodically elevated concentrations of organically bound nitrogen; hce – obligately nitrogen-heterotrophic taxa, needing

continuously elevated concentrations of organically bound nitrogen.

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164 Sophia Barinova et al.

3. Bio-indication of Water Quality

We constructed bio-indication plots on the base of ecological preferences of

the Kabul River species (Table 1) for revealed indicators distribution over major

environmental variables (Figures 4-6). Can be seen that number of species as well

as total number of each group indicators were sufficiently increase after the Swat

tributary input.

Figure 4. Bio-indicational plots in the Kabul River sampling stations of taxonomic

Division, Habitat preferences, temperature and oxygen.

Bio-indicational plots in Figure 4 show prevalence of benthic or

plankto-benthic species, temperate temperature indicators, and slow streaming

middle oxygenated waters.

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How water quality in the Kabul River, Pakistan… 165

Figure 5. Bio-indicational plots in the Kabul River sampling stations by salinity,

organic pollution according Watanabe, and according Sládeček indices, and

Classes of Water Quality.

Bio-indicational plots in Figure 5 show prevalence of salinity-indifferents,

eurysaprobes, III-IV Class of Water Quality that reflects middle polluted waters in

the Kabul River. The role of salinity in the riverine and especially lacustrine

community was studied during last year’s [38-41]. Usually salinity play the

negative role in algal species richness but here, in the Kabul River, we can see

that algal community was not suppressed and even stimulated down the river

because the chlorides come together with nutrients.

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166 Sophia Barinova et al.

Figure 6. Bio-indicational plots in the Kabul River sampling stations by trophic

state and type of nutrition.

Bio-indicational plots in Figure 6 show prevalence of mesotrophes,

autotrophic algae with tolerance to middle concentration of Nitrates. The

hydrological regime has both indirect and direct effect on aquatic community and

water quality through the changes of depth, nutrient concentrations, and water

volume. Generally, the symptoms of eutrophication of aquatic ecosystems are

more clearly manifested in periods of low water levels [42,43]. Here, in the Kabul

River, we can see that algal community was affected with water temperature and

nutrients, which increased down the river especially in the low-water periods of

autumn and spring. Therefore, studied part of the river can be characterized on the

base of bio-indication as middle polluted in the mesotrophic stage with tendency

of increasing of the eutrophication level. The same situation we can see in other

similar rivers which basins are in the Southern Eurasia regions such as Songhua,

Lower Jordan or Southern Bug [25,32-34,40]. Here integral bio-indicational

method for water quality and aquatic ecosystem sustainable assessment has been

represented relevant and stabile results, which can be employed in monitoring of

regional water quality.

3. Conclusion

Our results let us to conclude that firstly studied part of the Kabul River have

developed algal community with increasing of species richness and its abundance

in communities down the river. This process was stimulated not only the water

temperature increasing but also nutrients runoff from agricultural and domestic

activity in the Peshawar Valley and from the major tributary the Swat River. The

Swat River left high mountain tributary bring to the Kabul River its low enriched by major ions but more organically polluted waters. Algal community was increase in

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How water quality in the Kabul River, Pakistan… 167

species richness below the tributary input [44] as we can see in the rivers in the

climatically similar regions of Eurasia [32]. We revealed prevalence of green

algae and diatoms in studied algal community. The Charophyta species such as

filamentous Spirogyra and other filamentous algae were diverse and can be

represent some regional feature in the river basin with high agricultural activity

such as in China [32].

Water temperature can be characterized as one of the major variable that

stimulated riverine algal community. In other hand, water salinity was impacted

variable, which increased together with BOD and can be results of organic

pollution impact that come not only from industrial and agricultural activity in the

Peshawar Valley but also from the Swat River tributary as can be seen in the

bio-indication plots. The nitrates concentration was also important variable, which

together with temperature were affected riverine diversity in the Kabul River.

Bio-indication reflect arising of eutrophication level down the river but

calculated indices of saprobity S in the sites of studied part of the Kabul River

show high self-purification capacity of algal community. Therefore, we can to

conclude that integral and economy method of bio-indication for water quality

assessment can be employed in purpose of monitoring the regional water quality.

Acknowledgements. This work has been partly supported by the Israeli Ministry

of Absorption.

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Received: August 25, 2016; Published: October 11, 2016