Effect of water quality on the spatial distribution of charophytes in the Peshawar Valley, Khyber Pakhtunkhwa, Pakistan

The Peshawar Valley is a geographically important location in the Khyber Pakhtunkhwa province of Pakistan. The valley is located between 33.45′ and 34.30′N latitude and 71.22′ to 72.50′E longitude, at an altitude of about 345 m. The valley is girdled by mountains except its eastern side, where the Indus River forms a natural boundary. The center of the valley is a broad plain, generally level, but with occasional hills and rocky protuberances. The Peshawar Valley has a rich hydrography, including many rivers, streams and wetlands (Fig. 1). The Kabul River collects water from the streams and rivers of the Peshawar Valley and drains it into the Indus River near Attock (Government of Pakistan 1998). All water bodies in the Peshawar Valley were surveyed for the spatial distribution of charophytes and water quality effects, however, the studied algae were found at only 41 sites along the banks of seven rivers, 16 streams and two wetlands (Fig. 1). The geospatial location of each sampling site was recorded using a Garmin GPS Navigator (Table 1).

Figure 1

Charophyte specimens were collected at each sampling location within a 100 m radius by hand and using grapnels. Collected specimens were immediately preserved in situ with 5% FAA (formalin, acetic acid, and alcohol) solution in standard 500 ml specimen jars. Samples were labelled with a site code and stored in cardboard boxes to avoid spoilage (Edler & Elbrächter 2010). Micromorphology of charophytes was studied according to Urbaniak & Gąbka (2014). Specimens were places in Petri dishes and observed under an Olympus SZH stereo microscope using different magnifications (10× to 400×). Taxonomic identification of collected specimens was based on the standard literature of Urbaniak & Gąbka (2014), Wood & Imahori (1964), Pal et al. (1962), Prescott (1962), and Wood & Imahori (1959). To avoid using synonyms, the identified species were checked at www.algaebase.org. The conservation status and rarity of Charophyta species was assessed according to the IUCN criteria (IUCN 2012) using the following scheme:

The main physicochemical parameters of water quality (temperature, pH, oxidation reduction potential, electrical conductivity, resistivity, total dissolved solids, salinity and dissolved oxygen) were measured in situ in parallel with algae sampling at each sampling site using a HANNA HI-98194 multiparameter portable water quality meter (Khuram et al. 2019).

The map of the study area was prepared in ArcGIS version 10.8 using geospatial coordinates. A new statistical method of environmental mapping was used to visualize the environmental variables and species distribution using Statistica version 12.0 according to parameter values and geospatial coordinates of each site (Barinova, 2017). Canonical Correspondence Analysis (CCA) was used for multivariate direct gradient analysis to assess the effect of water quality on the spatial distribution of charophytes. Charophyta species richness data along with water quality data were analyzed using CANOCO version 4.5 (Ter Braak and Šmilauer, 2002). Comparative analysis of species abundance of microalgal communities accompanying charophytes was performed using BioDiversity Pro version 2.0.

In the Peshawar Valley, Chara braunii was found only in the Panjman Stream at the village of Panjman, the Swabi District (Figs 2, 3a). Langangen & Leghari (2001) also reported Chara braunii from the village of Nagar at the Karakoram Mountain range, from the town of Khwazakhela and the city of Mangora in the Swat Valley, which supports our results.

Figure 3

In our study, Chara connivens was found only in the Swat River at the city of Charsadda in the Peshawar Valley (Figs 2, 3b). Langangen & Leghari (2001) also reported Chara connivens from Lake Kinjhar in the Thatta District, which supports our results.

In the Peshawar Valley, Chara contraria was found in the Jindi River at the Tangi Harichand Road, in the Jindi River at the village of Prang Majoke, in the Indus River at the village of Galla, in the Naranji Stream at the village of Adina, in the Bada Stream at the village of Pabaini, and in the Badri Stream at the village of Mami Khel (Figs 2, 3c). Langangen & Leghari (2001) also reported Chara contraria from the Kotri pond, Lake Manchar, the village of Rani kot, the city of Sehwan, and the town of Thano bola in the Jamshoro District, which supports our results.

In our study, Chara globularis was found in the Naguman River at the village of Jalabella, in the Shah Alam River at the village of Michni, the Shah Alam River at the village of Shah Alam, the Swat River at the village of Munda, in the Abazai River at the village of Cheena, in the Jindi River at the village of Kanewar, in the Balar Stream at the village of Bakhshali, in the Bada Stream at the village of Pabaini, and in the Warsak Wetland at the village of Warsak, in the Peshawar Valley (Figs 2, 3d). Langangen & Leghari (2001) also reported Chara globularis from the village of Nagar at the Karakoram Mountain range, the Indus River at the city of Hyderabad, and Lake Kinjhar and the Sonda pond in the Thatta District, which supports our results.

In the Peshawar Valley, Chara vulgaris was found in the Kabul River (Warsak village), the Kabul River (Haji Zai village), the Naguman River (Niyami village), the Naguman River (Naguman village), the Shah Alam River (Shah Alam village), the Swat River (Dildar Gharhi village), the Jindi River (Tangi Harichand Road), Jindi River (Kanewar village), the Jindi River (Umarzai village), the Indus River (Galla village), the Indus River (Attock Khurd town), the Subhan Khwar Stream (Uchawala village), the Jalala Stream (Jalala village), the Jalala Stream (Mahabat Khan Koroona), the Uch Khwar Stream (Umar Abad village), the Bama Kandah Stream (Hathian village), the Ghargo Kandah Stream (Spalano Dheri village), the Lund Khwar Stream (Lund Khwar village), the Shamsi Dan Stream (Shamsi Dan village), the Shamsi Dan Stream (Said Abad village), the Balar Stream (Hamzakot village), the Balar Stream (Bakhshali village), the Balar Stream (Gari Kapura village), the Pacha Tangi Stream (Cheena village), the Dagi Stream (Hera Wand village), the Machi Stream (Machi village), the Gadar Stream (Katlang Road), the Naranji Stream (Turlandi village), the Naranji Stream (Adina village), the Naranji Stream (Sim Canal Road), the Bada Stream (Pabaini village), the Panjman Stream (Panjman village), Warsak Wetland (Warsak village) and Jamal Gharhi Wetland (Jamal Gharhi village, Peshawar Valley; Figs 2, 3e). Langangen & Leghari (2001) also reported Chara vulgaris from Lake Bakar in the Sanghar District, Lake Chatar in the Mirpur District, Hanna Lake in the Queta District, Lake Manjosa in the Poonch District, Lake Rawla (Islamabad), the Tarbella dam in the Swabi District, and at the villages of Kochalk, Rawla Kot, Tando Adam and Tando Mitha Khan, and in the Haripur and Peshawar Districts, which supports our results.

In our study, Nitellopsis obtusa was found in the Indus River at the village of Galla, the Peshawar Valley (Figs 2, 3f). Langangen & Leghari (2001) reported Nitellopsis obtusa from Lake Bakar in the Sanghar District, Lake Kinjhar in the Thatta District, and the Breja spring in the Dadu District, which supports our results.

The water temperature ranges from 10.32°C to 19.37°C, pH from 5.63 to 9.58, ORP from −50.8 mV to 236.2 mV, EC from 203 μS cm⁻¹ to 643 μS cm⁻¹, resistivity from 1555 Ω-cm to 4926 Ω-cm, TDS from 102 ppm to 326 ppm, salinity from 0.1 PSU to 0.32 PSU and DO from 2.22 mg l⁻¹ to 8.09 mg l⁻¹ (Table 2). The results showed that water quality parameters varied within a narrow range. They indicate that water at the surveyed sites was fresh, slightly saline, slightly alkaline and moderately saturated with oxygen. Water pH, EC, TDS, salinity and DO were within standard limits, while water temperature, ORP and resistivity showed deviations from good conditions (Wetzel 1983; Horne & Goldman 1994; Al-Badaii et al. 2013; Adhena et al. 2020; Alam et al. 2020). The sampling season, agricultural and nutrient runoff, domestic and industrial effluents were the major causes of fluctuations in water quality parameters, similar to previous studies conducted in habitats of the Upper Indus River (Ali et al. 2007; Barinova et al. 2013, 2016).

The distribution of the main environmental parameters is shown in Figure 4 in the form of statistically generated maps. Water temperatures in the studied water bodies were higher in small foothill rivers and streams (Fig. 4a). At only one site was the water pH below 7, reflecting the acidification impact (Fig. 4b). Salinity mapping showed that saline water was located in the valley plane (Fig. 4c). The highest dissolved water oxygen concentrations were found in several foothill habitats (Fig. 4d).

Figure 4

Canonical correspondence analysis (Fig. 5) showed that dissolved oxygen positively affected Chara vulgaris and negatively affected C. contraria and Nitellopsis obtusa. Chara braunii, C. connivens and C. globularis were positively affected by pH and resistivity, and negatively affected by total dissolved solids, electrical conductivity, and salinity. Temperature and oxidation reduction potential positively affected C. contraria and Nitellopsis and negatively affected C. vulgaris. Furthermore, CCA also revealed that total dissolved solids, electrical conductivity, and salinity have no effect on the spatial distribution of Chara contraria, C. vulgaris and Nitellopsis obtusa.

Figure 5

Statistical plots of Charophyta species in relation to water quality variables demonstrate habitat preferences of the identified Charophyta species (Figs 6, 7). Chara vulgaris demonstrated different preferences with respect to habitat parameters of the Peshawar Valley. Unlike other species, this species preferred more oxygenated water with elevated conductivity (Fig. 6), TDS, and salinity (Fig. 7). All six species preferred lower water temperature in the catchment of the Peshawar Valley (Fig. 7).

Figure 6

Figure 7

Comparative analysis of species abundance of microalgae communities associated with charophytes (Fig. 8) revealed high individuality of algae assemblages, as the percentage of similarity in Bray–Curtis analysis was below 25%. The most similar communities were those accompanying Chara contraria and Nitellopsis obtusa. The second similar pair were the communities of Chara globularis and C. vulgaris. The most distinct communities were those accompanying Chara braunii and C. connivens. Since microalgae communities show a clear response to the studied environment, we analyzed the distribution of Charophyta species in relation to environmental parameters (Figs 6, 7). Thus, in the pair of C. contraria and N. obtusa, which demonstrated similar preferences, the former species appears more indicative and can therefore be used as an indicator for this pair. Although, the communities of C. globularis and C. vulgaris were similar, the preference profiles were unique for each species (Figs 6, 7). At the same time, C. braunii and C. connivens have the same preferences for environmental parameters of waterbodies in the Peshawar Valley. Therefore, in this pair, both species can serve as indicator species.

Figure 8

The Charophyta species analyzed in this study were usually assessed not only as indicators of environmental quality but also as indicators of threats to algal communities. Charophytes make up the majority of algae biomass in most habitats, but if one species is endangered, the entire community is threatened. Since Pakistan does not yet have a Red List of Endangered Species, our results will serve as a basis for developing such a list for aquatic species. We compared the six species studied with the Red Lists of Balkans, Poland, Ukraine, the Czech Republic, and Germany in terms of the IUCN risk categories (Palamar-Mordvintseva & Tsarenko 2004; Blaženčić et al. 2006; Caisova & Gąbka 2009; IUCN 2012; Becker et al. 2016). We found that Chara braunii, C. contraria, C. globularis and C. vulgaris can be classified as being at low risk of extinction (LR). C. connivens is endangered in the Balkans and threatened with extinction in Poland (EN). Nitellopsis obtusa is a regionally very rare species and has a disjunctive distribution worldwide. It occurs in water bodies in various countries of Europe and Asia. In Europe, it is classified as at high risk of extinction (VU). However, the determination of the VU category for this species in the flora of Pakistan requires additional argumentation and factual material on its vulnerability, which can be found in the Red List of Algae compiled for Pakistan.

It is known that pH, conductivity, salinity, total hardness, carbonate hardness, total phosphorus, total nitrogen, ammonia nitrogen are important for charophytes in European habitats (Becker et al. 2016). In Europe, Nitellopsis obtusa prefers slightly alkaline or neutral water, C. globularis and C. contraria thrive better in brackish water with high conductivity, C. contraria, C. globularis, C. vulgaris, and Nitellopsis obtusa tolerate moderate organic pollution. We confirmed that rare Nitellopsis obtusa in the ecosystems of the Peshawar Valley prefers low alkaline waters with low temperature, low salinity and low TDS, which extends the ecology of this species. Since Nitellopsis was recorded at only one site (Fig. 3f), the species was classified as VU. Chara contraria communities were paired with Nitellopsis classified as VU, because they avoid polluted waters at the inlet of the Swat and Kabul rivers into the Peshawar Valley (Fig. 3c,f), which was also reported from Poland (Blaženčić et al. 2006). C. vulgaris and C. globularis, on the other hand, were more common in the Peshawar Valley (Fig. 3d,e). They prefer slightly contaminated water bodies. Therefore, neither of the species in this pair could be included in the IUCN conservation categories in our study area. The last pair of species with similar community responses to the environment are C. braunii and C. connivens, both of which are rare in the Peshawar Valley. Both species prefer low saline and low alkaline waters and avoid polluted areas as Nitellopsis. This allows us to assign them to categories from LR to EN, as in Europe.