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Phytophilous macroinvertebrate assemblages in Nigeen lake of Kashmir

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Article in Tropical Ecology · January 2024

DOI: 10.1007/s42965-024-00341-0

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Tropical Ecology International Society
https://doi.org/10.1007/s42965-024-00341-0 for Tropical Ecology

RESEARCH ARTICLE

Phytophilous macroinvertebrate assemblages in Nigeen lake of

Kashmir Himalaya
Shahid Ahmad Dar1 · Sayima Gulzar1 · Sami Ullah Bhat1

Received: 28 September 2022 / Revised: 8 August 2023 / Accepted: 5 January 2024

© International Society for Tropical Ecology 2024

Abstract
Macroinvertebrate assemblages associated with six aquatic macrophyte species were investigated in Nigeen Lake of
Kashmir valley, Jammu and Kashmir. Across the lake surface, four locations were selected for collection of the aquatic
macrophytes. The macrophytes were collected in plastic bags, labelled, and brought to laboratory for further analysis.
The samples were sieved using a 0.5 mm mesh, sorted, and identified. During the study period, 18 macroinvertebrate
species were recorded from 6 macrophytes. The macroinvertebrates belonged to eight families, seven orders, and extend
over three phyla, viz.: Mollusca, Arthropoda, and Annelida. Phylum Arthropoda comprised of highest number (11) of
species, followed by Mollusca (4), and Annelida (3). Maximum number of individuals was found attached to Myriophyl-
lum verticillatum (75 ind./m2), Potamogeton crispus (71 ind./m2), Trapa natans (60 ind./m2), Potamogeton natans (57
ind./m2), Ceratophyllum demersum (38 ind./m2), and least for Potamogeton lucens (19 ind./m2). Principal component
analysis (PCA) of the data resulted in two principal components (PCs) with eigenvalues > 1, explaining 86% of variance.
Investigation of the factor loadings of macroinvertebrate assemblages linked with aquatic macrophytes on the first two PCs
of the dataset revealed that relationship exhibit habitat gradients potentially affecting associated macroinvertebrates. The
study demonstrated that macroinvertebrates differed with different vegetation types in terms of both density and diversity,
and that plant structure plays a significant role in determining this variation. Macroinvertebrate communities benefit from
increased macrophyte productivity. The study concludes that the certain taxa of macroinvertebrates are more comfortable
to the high pollution loads and nutrient enrichment in the Nigeen lake.

Keywords Annelida · Arthropoda · Kashmir valley · Nigeen lake · Macroinvertebrates · Macrophytes

Introduction aquatic invertebrates which live on or inside tissues of

aquatic macrophytes (Feldman 2001). The abundance and
Macrophytes are essential components of aquatic eco- richness of macroinvertebrates is higher in areas having
systems (Bhat et al. 2012; De et al. 2019). Besides being dense macrophyte vegetation compared to the unvegetated
the indicators of pollution of water bodies (Baturina and habitats (Alonso and Camargo 2010). In addition, different
Fefilova 2021), they play an important role in structuring aquatic plant species support different assemblages of plant-
the biotic communities in aquatic environments (Thomaz associated invertebrates (Gallardo et al. 2017). The macro-
and Cunha 2010). Aquatic macrophytes provide food, phys- invertebrates live in close proximity to the shoots and leaves
ical support, add to habitat heterogeneity, complexity, and of the aquatic macrophytes. The relationship between mac-
influence diverse organisms like macroinvertebrates, fishes, rophytes and invertebrates can either be for food, for egg
and water birds (Thomaz and Cunha 2010; Divya and San- laying, and for protection from predator organisms (Walker
ilkumar 2021). Phytophilous macroinvertebrates are those et al. 2013).
Characteristics and abundance of macroinvertebrates is
inflated by an array of factors, the ones which change the lit-
toral habitats in some or other way being the most important
Sami Ullah Bhat
[email protected] (Prokin and Seleznev 2021). However, aquatic macrophytes
have a distinctly diverse architecture and growth pattern,
1
Department of Environmental Science, University of which was expected to control macroinvertebrate density,
Kashmir, Srinagar-190006, Kashmir, J&K, India

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occurrence, and size of the individuals (McAbendroth et and community structure of phytophilous macroinverte-
al. 2005). Architecture type of macrophytes explains some brates in Nigeen lake, Jammu and Kashmir, India. We
of the variations in the diversity and abundance of macro- hypothesized that (i) some macroinvertebrate species are
invertebrate communities (Feldman 2001). Aquatic mac- more sensitive to pollution than others, with the increase
rophytes having fine vivisect leaves hold-up large number in pollution levels, pollution tolerant species survive; (ii)
of macroinvertebrates as compared to other plants having the macrophyte architecture has a direct influence on the
undissected broader foliage (Andrews and Hasler 1943). density and diversity of macroinvertebrates. The objec-
Phytophilous macroinvertebrates act as bioindicators of the tives of the present study are (i) to investigate the macro-
hydrological regimes, water quality status and are the key phytes present in Nigeen lake, (ii) to assess the diversity
components for smooth functioning of aquatic ecosystems and community structure of macroinvertebrates attached
(Kratzer 2002). to macrophytes, and (iii) to find the influence of mac-
Nigeen Lake is an urban ecosystem in the Srinagar city rophyte architecture on the macroinvertebrate diversity
of Kashmir valley (Nabi 2021). The lake supports impor- and density. The information derived from the study is
tant ecosystem services and livelihood opportunities for crucial for managers and policy makers to make informed
local populations. The lake is known for its aesthetics, decisions towards improving the ecological health of the
houseboats, scenic beauty, and socio-economic activi- Nigeen lake ecosystem.
ties. Although numerous studies have been conducted
on Nigeen lake including the hydrochemistry and land
use land cover changes (Dar et al. 2020a), density and Materials and methods
diversity of phytoplankton assemblages (Nissa and Bhat
2016), and zooplankton communities (Jan et al. 2015) but Study area
there has been no such study focusing on the phytophi-
lous macroinvertebrate community in Nigeen lake. Nigeen lake is an offshoot from Dal Lake (Nissa and Bhat
The main rationale behind the study is that the mac- 2016), situated at a distance of about 09 km on north-
roinvertebrates form the essential constituent of Nigeen eastern part of Srinagar, between 34°06ʹ & 34°07ʹN lati-
lake biodiversity and effectively reveal the status of eco- tudes and 74°49ʹ & 74°50ʹE, longitudes at an elevation
logical health of the ecosystem. However, freshwater of about 1584 m amsl (Fig. 1). The lake has a surface
biodiversity in the Nigeen lake is facing multiple anthro- area of 1.38 km2 (Dar et al. 2020a). The total volume of
pogenic pressures from population increase, houseboats, the lake is calculated as 1.22 × 106 m3. The Lake is con-
dense human settlements, tourism, and commercial agri- nected to Dal Lake at Ashai bagh. The water supply is
culture. These activities have led to an increase in both maintained by a narrow water channel of Dal Lake, in
organic and inorganic pollutants (e.g., nutrients such as addition to springs within the lake and atmospheric pre-
nitrates and phosphates, and heavy metals such as copper, cipitation, and domestic effluents being the other sources
cobalt, and nickel) affecting the health of lake ecosystem of water. Nigeen Lake drains into Khushalsar via Nallah
(Nabi 2021). The lake has also been subject to distur- Amir Khan (Dar et al. 2020b, 2021a). Also, a long chan-
bance by weed harvesters and dredgers which can affect nel to the southwest of Nigeen Lake drains water into
taxa richness. Similarly, anthropogenic activities, such as river Jhelum via Brari Nambal wetland (Dar et al. 2023).
sewage disposal from houseboats and nearby settlements Nigeen being an urban lake, like other lakes and wetlands
could contaminate the ecosystem. The anthropogenic dis- of Kashmir valley (Dar et al. 2022; Rashid et al. 2023)
turbances in the form of sewage disposal and macrophyte is subjected to excessive biotic pressures and receives
harvesting can impact the ecology of the lake ecosystem large quantities of untreated sewage from houseboats and
(Rather et al. 2020). Changes in water quality and nutri- residential hamlets within the lake (Dar et al. 2021b, c,
tional resource base may affect the relative abundance, d). The lake is invaded by dense macrophytes both sub-
diversity and composition of macroinvertebrate species. merged and free-floating forms.
Ultimately the change in the composition of macroinver-
tebrate species could result in a change in the composition Study locations
of species at higher trophic levels like fishes. This could
also pay a way for the establishment of non-native spe- The study aimed at having a comprehensive knowledge
cies as very recently the non-native species Alligator gar of macroinvertebrates associated with lake macrophytes.
(Atractosteus spatula) native of North America has been During surveys in the lake ecosystem, it was observed
found in the Dal Lake. Therefore, this study is an attempt that the macrophytes grow in patches with each patch
to provide a comprehensive picture of the density pattern comprising of only one or two species of macrophytes. As

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Fig. 1 Map of Nigeen Lake showing the sites selected for collection of samples

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a result, study locations in different macrophyte patches of 34°06ʹ26.51ʺN latitude and 74°49ʹ51.70ʺE longitude.
were selected in order to cover all the different species The macrophyte communities at this site include Myrio-
of macrophytes in the lake ecosystem. Across the lake phyllum verticillatum., and Potamogeton natans., This
surface, four study locations were selected (Fig. 1), the site is surrounded by residential buildings and floating
detailed description of the study locations is presented gardens.
below.

Location I This site lies on the southeast of the lake Collection and identification
between the geographical coordinates 34°06ʹ52.56ʺN
latitude and 74°50ʹ08.36ʺE longitude. The macrophyte The macrophyte samples were collected from four sampling
communities include Potamogeton crispus., and Cerato- locations in the Nigeen lake for a period of four months. In
phyllum demersum. the Kashmir valley, the spring season is characterized by
low temperatures in which macrophytes start growing. In
Location II This site lies on the central east portion of the the summer and autumn season, macrophyte communities
lake between geographical coordinates 34°07ʹ14.00ʺN achieve their optimum growth and in the late autumn their
latitude and 74°49ʹ58.67ʺE longitude. This site is sur- death and senescence take place. Therefore, the samplings
rounded by houseboats and is completely covered by the were carried out in summer (June and July), and autumn
luxuriant growth of Trapa natans. (October, and November) season. Further biomonitoring
data obtained in summer and autumn season most represen-
Location III The site lies on the center of the lake between tatively reflects the ecological state of aquatic ecosystems
the geographical coordinates of 34°07ʹ16.40ʺN latitude (Bazhenova and Mikhailov 2021).
and 74°49ʹ47.51ʺE longitude. This site dominantly sup- For achieving the objectives of the study, six macrophytes
ports the growth of Potamogeton lucens., besides, few based on their presence in the Nigeen lake were selected.
patches of algal mats are also present at this site. These include Potamogeton crispus, Ceratophyllum demer-
sum, Trapa natans, Potamogeton lucens, Myriophyllum ver-
Location IV This site lies on the southwest of the Lake ticellatum, and Potamogeton natans, (Fig. 2). The collection
near Khoujyarbal area between geographical coordinates of aquatic macrophytes was done using a handmade sampler

Fig. 2 Macrophyte species collected from Nigeen lake a Potamogeton natans, b Myriophyllum verticillatum, c Potamogeton crispus, d Cerato-
phyllum demersum, e Potamogeton lucens, and f Trapa natans

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in which a hook was fitted with an iron rod (Javaid et al. 2023). The method works with a correlation matrix and thus
2018). The sampler was dipped in water column and moved reflects the stochastic interdependencies.
to cut the macrophytes. The sampler was taken out from the
water column and the aquatic macrophytes attached with
the sampler were collected and transferred into collection Results
bags. In the laboratory, the samples were segregated, of each
macrophyte was taken in a sampling tray. The tray was filled Overall, 18 macroinvertebrate species were recorded from
with water and the macrophytes were vigorously shaked to 6 aquatic macrophytes of the lake. The species belonged to
free attached macroinvertebrates. The water was passed eight families, seven orders, and three phyla namely Mol-
through a sieve having a size of 0.5 mm to collect the macro- lusca, Arthropoda, and Annelida (Table 1). Arthropoda
invertebrates. The macroinvertebrates were picked up from was the most dominant taxa and comprised of 11 taxa
the sieve with a fine camel hair brush and were preserved in represented by only 1 class Insecta. Class Insecta contrib-
4% formaldehyde in a properly labelled photographic film uted majority of class forms with 10 taxa belonging to 5
vials. The identification of the macroinvertebrates was done different orders (Diptera 4, Amphipoda 2, Coleoptera 1,
by the help of published keys of Pennak (1978) McCafferty Odonata 1, and Crustacea 1). Mollusca were represented
and Provonsha (1998), Wetzel and Likens (2000). by 4 taxa (Physella, Lymnea ovata, Gyralus, and Lymnea
auricularia). Annelida was represented by 1 taxon (Erbop-
Statistical analysis della). Among 18 taxa of macroinvertebrates, Insecta were
the most dominant. The Chironomidae larvae were much
Various statistical methods such as Tukey’s test and Homo- more diverse showing higher density on Potamogeton cri.,
geneity of Variance (Levene’s test), and principal compo- followed by Potamogeton lucens, and Myriophyllum ver-
nent analysis (PCA) were applied to the datasets. Tukey’s ticellatum. Mollusca prosper in aquatic systems having
test and Levene’s test were applied to identify and verify high temperature and calcium enriched waters and showed
whether significant variance across groups or samples occur their presence on Potamogeton crispus, followed by Trapa
respectively. PCA is an important stochastic method used natans, and Ceratophyllum demersum, as a result of cal-
to decrease the dimensionality of interrelated variables of cium carbonate depositions on the leaves and large surface
a dataset by converting unique, interrelated parameters area of the macrophytes. The highest density was observed
into a few orthogonal (uncorrelated) parameters known as on Trapa natans, followed by Myriophylum verticellatum,
principal components (PCs) (Islam et al. 2021; Dar et al. Potamogeton natans, and least for Potamogeton crispus,
Potamogeton lucens, and Ceratophyllum demersum. Myrio-
phyllum verticellatum, was found to harbour 8 taxa belong-
ing to phylum Arthropoda, Annelida, and Mollusca. The
Table 1 Community structure of phytophilous macroinvertebrates
found in Nigeen Lake density of Chironomidae sp. was reported to be higher on
Phylum Order Family Genus Myriophyllum verticellatum, as compared to other macro-
Annelida Hirudinea Erpobdellidae Erpobdella sp. phytes. Phylum Mollusca was found to be absent on Pota-
Erpobdella sp. mogeton natans.
Erpobdella sp. During the present study, macroinvertebrate assemblages
Mollusca Gastropoda Lymnaeidae Lymnaea associated with different macrophytes differed consider-
auricularia ably. Maximum number of individuals was found attached
Lymnaea ovata
to Myriophyllum verticellatum, (75 ind./m2), followed
Planorbidae Gyraulus sp.
by Potamogeton crispus, (71 ind./m2), Trapa natans, (60
Physidae Physella sp.
ind./m2), Potamogeton natans, (57 ind./m2), Ceratophyllum
Arthropoda Trichoptera Hydroptilidae Hydroptilidae sp.
Diptera Chironomidae Epididae sp.
demersum, (38 ind./m2), and least for Potamogeton lucens,
Chironomidae (19 ind./m2) (Fig. 3). The percentage contribution of dif-
sp. ferent macroinvertebrates on six macrophytes showed the
Diamesinae sp. order: 23% on Myriophyllum verticellatum, 22% on Pota-
Ceratopogonidae Probezzia sp. mogeton crispus, 19% on Trapa natans, 18% on Potamoge-
Odonata Coenagrionidae Enallagma sp. ton natans, 12% on Ceratophyllum demersum, and 6% on
Coleoptera Elmidae Elmidae sp. Potamogeton lucens (Fig. 4).
Dytiscus sp. The comparison plot between the collected macroinver-
Beetle sp.
tebrates i.e., the mean population was not significantly dif-
Amphipoda Gammaridae Gammarus sp.
ferent at p < 0.05 across the different vegetation types (Fig.
Araenaea Pisauridae Dolomedes sp.

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Fig. 3 Abundance of macroinvertebrates associated with different macrophytes

Fig. 4 Number of species (%) associated with different macrophytes

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Fig. 5 Biplot of macroinvertebrates associated with different vegetation types

Table 2 Loadings of variables on the first two principal components

derived from PCA of macroinvertebrate phyla associated with differ- other orders tend to increase as well. The correlation value
ent vegetation types (Boldfaced values, were considered high) of 0.896, shows abundance of Annelida. The second PC has
Macroinvertebrate Phyla PC1 PC2 strong positive loadings from the Mollusca and negative
Arthropoda 0.634 -0.699 loadings from the Arthropoda. This means that the second
Annelida 0.896 0.002 principal component increases with increase in Mollusca
Mollusca 0.601 0.734
and decrease in Arthropoda order.
Eigenvalues 1.569 1.028
Variability (%) 52.3 34.2

Discussion
S1). Whereas the homogeneity variance test of the popu-
lation variance is significantly different at p < 0.05 across The variation in richness and abundance of macroinver-
different vegetation types (Table S1). The principal compo- tebrates on various aquatic macrophytes is most likely
nent analysis of the data resulted in two PCs with eigen- determined by a range of factors like morphology of the
values > 1, explaining 86% of variance (Fig. 5; Table 2). macrophytes, growth of periphyton, invertebrate behavior,
The first PC explained a variance of 52.3% with highly competition, and predator-prey relationships (Taniguchi et
strong positive loadings from Annelida and strong positive al. 2003; Šetlíková et al. 2016). Additionally environmental
loadings from species of Arthropoda and Mollusca. The factors like temperature, water flow, and quality of water act
first principal component shows increase with increase in as determinants for macroinvertebrates growing on various
Annelida, Arthropoda, and Mollusca. This suggests that macrophyte species (Strayer et al. 2003). During the study
the three orders vary together. If one order increases, the period, Arthropoda were highly diversified than Mollusca

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and Annelida. However, the mean density of Arthropoda al. 2008). On the other hand, emerging and floating mac-
was low, this is attributed to the fact that most of the insect rophytes have been linked to higher primary productivity
communities spend a small time period of their life-cycles than submerged macrophytes (Lycarião and Dantas 2017).
as larva in aquatic ecosystems and afterward come out as According to Damanik-Ambarita et al. (2016), macrophyte
adult beings, occupying terrestrial habitats as aerial beings productivity can have a favourable impact on macroinverte-
(Albertoni et al. 2007; Baron and Ostrofsky 2010). The brate communities.
highest abundance of macroinvertebrates on Myriophyllum The studied macrophytes are the prominent ones found
verticellatum, may also be related to the high availability in the Nigeen Lake. These macrophytes provide valuable
of nutrients and ions to the macroinvertebrates. The Myrio- habitat, food source, and are populated by a multiplicity of
phyllum verticellatum, grows at location IV (Khoujyarbal), macroinvertebrates (Strayer and Malcom 2007). Although
Dar et al. (2020a) has reported higher concentration of vari- macrophytes do not come out to have a distinctive macro-
ous nutrients and ions such as ammonical nitrogen, sodium, invertebrate species associated. Submerged macrophytes
potassium, phosphorus, and chloride at this location in the offer different substratum’s that can be used by different
Nigeen lake. Chironomous sp. was the dominant group species of macroinvertebrates (Christoffersen 2008). The
and showed higher density on Potamogeton crispus., fol- high density of macroinvertebrates on Potamogeton cris-
lowed by Potamogeton lucens, and Myriophyllum verticel- pus, may be due to the possibility that Potamogeton cris-
latum. These macrophytes prefer to grow in polluted waters pus, supports more algae than other macrophytic species
enriched with nutrients as also reported by Chowdhary et (Mohamed 2017). The comparison plots showed how mac-
al.(2013). Molluscs rely on calcium for growth of their roinvertebrates varied differently with different vegetation
shell and so are highly dependent on calcium availability types both in terms of density as well as diversity. Investiga-
for survival, demonstrating reduced growth rate, survival tion of the factor loadings of associated macroinvertebrates
and reproductive output in low calcium environments (Zal- with aquatic macrophyte species on the first two PCs of the
izniak et al. 2009). In high calcium environments Molluscs data set revealed that relationship exhibit habitat gradients
can demonstrate induced shell thickening in the presence potentially affecting associated macroinvertebrates. Due to
of predators, potentially reducing predation mortality; an overall poor habitat quality phytophilous macroinverte-
however, this induced response is prevented when calcium brate community in Nigeen lake was represented by species
availability is limited (Rundle et al. 2004; Czarnoleski et al. thriving well in organic and nutrient rich water. These find-
2006). ings are in agreement with the works of Habib and Yousuf
The richness of macroinvertebrates was found positively (2016) who reported pollution tolerant species while work-
associated with abundance of macrophytes and sediments ing on phytophilous macroinvertebrate assemblages in Dal
rich in organic nutrients. Zelnik et al. (2018) confirmed Lake of Kashmir valley.
significant positive correlations between diversity of mac-
rophytes and macroinvertebrates while working on karst Ecological significance of the study
ponds of SE Alps Slovenia. The abundance of phytophi-
lous macroinvertebrates was found to be greatly determined Biological approaches for identifying natural and anthro-
by architecture of macrophytes. Macrophytes with a large pogenic impacts on lake ecosystems are important because
surface area were found to favor large number of macro- biota responds to stresses from many geographical or tem-
invertebrates. Surface area, leaf morphology, and chemical poral dimensions. Additionally, the biological community
secretions of aquatic macrophytes have a significant effect incorporates structural and functional properties and pro-
on the overall abundance and diversity of macroinverte- vides a reliable indicator of the health of the lake ecosys-
brates associated with different macrophytes (Rezende et tem. Studying macroinvertebrates in ecological research has
al. 2019). The results indicated a significant dissimilarity in shown to be more successful than relying just on environ-
macroinvertebrate fauna associated with different aquatic mental factors. The richness and composition of macroin-
macrophytes mainly because of progression in age group of vertebrate species reported in the study have been utilized
dominant macroinvertebrate fauna (Dvorak and Best 1982). to draw insights about the levels of organic pollution in the
In terms of plant architecture and surface area, submerged Nigeen lake. The existence of pollution-tolerant species is
macrophytes often have a higher level of morphological an important finding of the study indicating human influ-
complexity than emergent macrophytes (Thomaz and Cunha ences and a shift in the composition of macroinvertebrates
2010). Because emergent macrophytes are less complicated in the lake ecosystem. The pollution-tolerant macroinver-
than submerged macrophytes, they may support macroin- tebrates facilitate the growth and establishment of higher
vertebrate communities with lower biomass, different spe- species that are likewise resistant to pollution. The Alligator
cies compositions, and various size structures (Tessier et gar was very recently found in Dal Lake of which Nigeen

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manuscript to be published
lake is a subsidiary basin and it shows the presence of
specific stresses on lake ecosystem such as low dissolved Competing interests The authors declare that they have no conflict
oxygen, sewage, high pollution loads etc. As a result, stress- of interest.
impacted Nigeen lake tend to lose sensitive native species
and their replacement by stress-tolerant native or exotic
species. Ultimately the various forms of stress result in References
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Acknowledgements The authors thank the Department of Environ- als P (2016) Generalized Linear models to identify key hydromor-
mental Science, University of Kashmir for providing laboratory facili- phological and chemical variables determining the occurrence of
ties and bearing the expenses of hiring the motor boat for collection Macroinvertebrates in the Guayas River Basin (Ecuador). Water
of samples in the Nigeen Lake. Authors wish to extend their gratitude 8(7):297. https://doi.org/10.3390/w8070297
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Funding The authors have not received any funding for carrying out s10661-020-8091-y
this study. Dar SA, Bhat SU, Rashid I, Dar SA (2020b) Current status of wet-
lands in Srinagar City: threats, Management Strategies, and future
Data availability The datasets generated during and/or analyzed dur- perspectives. Front Environ Sci 7:1–11. https://doi.org/10.3389/
ing the current study are available from the corresponding author on fenvs.2019.00199
reasonable request. Dar SA, Rashid I, Bhat SU (2021a) Land system transformations gov-
ern the trophic status of an urban wetland ecosystem: perspectives
from remote sensing and water quality analysis. Land Degrad Dev
Declarations 32:4087–4104. https://doi.org/10.1002/ldr.3924
Dar SA, Bhat SU, Rashid I (2021b) The Status of Current Knowledge,
Ethics approval and consent to participate Research ethics stand ad- Distribution, and Conservation Challenges of Wetland Ecosys-
hered while submitting the manuscript. All the authors approved the tems in Kashmir Himalaya, India. In (eds S. Sharma and P. Singh),

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