Introduction

The valley is a unique natural region, lying within the north western tip of oriental region abutting the Palaearctic region, between 33°25′–34°50N′ and 74°–75.5′E. In the western Himalaya, the high altitude valley of Kashmir abounds in a vast array of freshwater bodies including lakes, wetlands, springs and streams [1–3]. Among these the lentic ecosystem (lakes and wetlands) assume significant importance in being greater repository of freshwater biodiversity which is generally understood largely due to the result of increasing human pressure [4–7]. Rotifers were first studied by Leuwenhoek in the year 1703. Rotifers are pseudocoelomate living creatures, ranging from 50 to 2,000 mm in size. It is one of the oldest groups of invertebrates in nature [8]. The general body plan of a rotifer consists of three basic regions (corona, trunk and foot). In many species corona consists of trochus and cingulum (two rings of cilia that beat in a metachronous pattern). The trunk is divisible into five parts namely mouth, mastax, stomach, intestines and anus while the foot consists of pseudo segments and toes [9, 10].

They have achieved more significance in freshwater by residing in littoral, limnetic and benthic regions [11–13], and most of them are cosmopolitan in distribution [14, 15]. The phylum Rotifera comprises approximately 2,030 described freshwater species from the world [16]. It has been divided into three classes: Monogononta (1,570 species) being entirely parthenogenetic, Bdelloidea (460 species), and Seisonidea with a few species (two known genera with three species). Former two have been recognized as freshwater classes and the latter one as marine [16–19]. Rotifers play a major role in energy relocation and nutrient cycling [20], and are often used as bioindicators of water pollution [21–23]. The community composition and density of rotifers greatly varies with degree of eutrophication [24, 25]. They have also been reported as bioassay animals [26]. Further, rotifers have gained great ecological importance in aquatic environments by adopting the method of filter feeding by consuming and incorporating different types of food resources of different sizes [13, 27, 28].

Taxonomic Survey of Rotifera in India

According to a conservative estimate, there are over 500 species of rotifers in Indian water bodies, although only 330 species belonging to 63 genera and 25 families have so far been authenticated [29]. Segers and Babu [30] and Sharma and Sharma [31] have added 5 new taxa to the Indian checklist. Taxonomic work in India was initiated by Anderson [32] who listed ten new species from Calcutta while Murray [33] listed 32 species from the Sikkim Himalaya. In another survey, Steward [34] reported 17 species from trans-Himalayan region. During the Yale of North India Expedition, Edmondson and Hutchinson [35] reported 100 species including 13 species of the family Lecanidae from different localities of India. Ahlstrom [36] described two new species, Keratella quadrata var. edmondosoni and K. quadrata var. pyriformis from Madras. Nayar and Nair [37] described 15 brachionid rotifers first time from Kerala with four new reports as Brachionus forficula keralaiensis, Dipeuchlanis propatula, Anuraepsis fissa lata and B. caudatus personatus). Nayar [38] while studying Rotifer fauna of Rajasthan reported 36 species, of which 14 species were reported for the first time in India including one new species.

Other notable contributions in this field were that of Naidu, [39], Vasisht and Gupta [40], Vasisht and Battish [41, 42] and Sharma, [43–48]. However, Sharma and Micheal [49, 50] prepared a taxonomic list of Indian rotifers by extensive surveys from different parts of the country but the species exiting in Kashmir Himalaya were not fully explored though later on Wanganeo and Wangeneo [51] and Pandit [52] have provided a detailed list of rotifer species from the Kashmir Himalayan region (Table 1). Sharma and Micheal [49] confirmed the presence of 241 species of rotifers from the Indian subcontinent. Subsequently, 60 more species have been added to the list [52–55].

Table 1 List of rotifer species recorded from freshwaters of Kashmir Himalaya: an overview
Full size table

Seasonal Variation in Rotifer Community

Environmental variation is one of the fundamental factors that determines the life patterns of an organism. Temperature is one among of the prominent factors governing the chemistry of surrounding environment [56]. Therefore, species to remain alive must adopt the broad range of different environmental conditions. As a result certain conditions become maladaptive for many species or adoptive for remaining species, the adaptability giving rise to different seasonal succession patterns [57]. Seasonal variation of rotifers were studied by various authors in Kashmir and different parts of India. [4, 58–60]. However, the research scenario of rotifers in Kashmir is fully not well established and majority of the reports pertain to only spatial and temporal variations.

Taxonomic survey of rotifers in Kashmir was started by Edmondson and Hutchinson [35] who reported only eight species from lake Manasbal. After the gap of more than three decades, taxonomic work was reinitiated by Das [61], Das and Akhtar [62] and Zutshi et al. [63] who while studying the comparative limnology of nine lakes of Jammu and Kashmir reported that rotifers were the main component of the zooplankton community, Keratella cochlearis being the dominant species, among the 16 taxa reported while Ascomorpha eucaudis showed restricted distribution to only one biotope (Dal lake). Kaul et al. [64] reported 18 rotifer species from the freshwater bodies of Jammu and Kashmir, highest being recorded from sewage pond, with the dominance of Brachionus calyciflorus, reflecting high tolerance limit towards pollution. In another study Zutshi et al. [65] found only one species (Euchlanis dilatata) in spring and summer season. Seasonal abundance of rotifera in lake Manasbal was carried out by Yousuf and Qadri [66, 67] who reported 38 species of rotifers belonging to eleven families, with varied population peaks in littoral zones, while bimodal pattern of population growth (late summer-early autumn and late winter-early spring) was recorded in the limnetic stations. Zutshi and Vass [68] reported 37 species of rotifers among 93 zooplankton species in Dal lake showing maximum population density in spring and late summer. In Mirgund wetland Rotifera emerged as the most dominant group in terms of both taxa and population [69]. Euchlanis dilatata was the most dominant rotifer species among 18 species of rotifers. Khan [70] reported 27 rotifers, among 51 taxa of zooplankton, exhibiting bimodal population peaks throughout the study. A detailed hydrobiological study of Anchar lake was carried by Balkhi et al. [71] reporting 41 species of rotifers, with Asplanchna priodonta being the most dominant species. Pandit and Qadri [72] while studying the wetlands of Kashmir opined that severe floods often lead to increase in rotifers particularly Brachionus sp. and Keratella sp.

Pandit [4] while studying trophic structure of plankton community in some typical wetlands of Kashmir reported 141 species of zooplankton, of which 29 belonged to rotifera. The author opined that rotifers contribute very low towards the zooplankton standing crop as compared to crustacea and protozoa. Mean biomass was registered highest (1.22 mg/m3) for Mirgund followed by Nowgam (1.14 mg/m3) Haigam (1.04 mg/m3) in Malgam (0.84 mg/m3) and Hokarsar (0.43 mg/m3) in a decreasing order. Among the five studied wetlands of Kashmir, Nowgam, Malgam, Hiagam, Mirgund and Hokarsar, the dominant rotifer genera were Keratella, Brachionus, Cephalodella, Monostyla, Lecane, Synchaeta, Asplanchna, Trichocera, Filina and Mytilina. Pandit and Yousuf [73] while studying the rotifer community in some Kashmir Himalayan lakes of varied tropic status observed 98 species of rotifers. They further opined that rotifer community increased qualitatively as well as quantitatively from oligotrophic to mesotrophic then finally to eutrophy. Species which were dominated in oligotrophic lakes were Asplanchna priodonta and Kellicotia longispina, while Brachionus calyciflorus and B. quadridentata were significant in hypereutrophic waters of Khushhalsar lake.

Siraj et al. [74] reported 32 species of rotifers among 65 zooplanktons around floating gardens in the Dal Lake. Wanganeo et al. [75] while studying the seasonal variation of rotifers in relation to physico- chemical parameters identified 47 rotifer species, showing unimodal growth peak of density in summer and further inferred that rotifer populations showed significant positive correlation with temperature, nitrate, chloride and phosphate and negative correlation with dissolved oxygen throughout the entire study period.

Relation with Abiotic Parameters

In an aquatic ecosystem the life of biota is closely dependent on the physical, chemical and biological characteristics of water, some of which directly act as the controlling factors. Therefore, for understanding the dynamics of an organism, a population or a community, knowledge of both the organism and its environment is important [76]. Yousuf and Qadri [66] while studying seasonal abundance of rotifera in a warm monomictic lake categorized the species into perennial (Polyarthra sp., Synchaeta sp., Asplanchna sp., Monostyla sp. and Keratella sp.) and seasonal with warm stenothermal (Brachionus sp., Anuraeopsis sp.) and cold stenothermal (Filinia sp., Notholca sp., Proales sp. and Bdelloid sp.). Qadri and Yousuf [77] while studying two rotifer species Anuraeopsis fissa Gosse and Notholca acuminate Ehrn opined that the former species prefers carbonate water and a narrow range of temperature (18–25 °C) with complete establishment of thermocoline in the lake, while the latter species was reported to be a cold stenothermal with peak population in the month of February, besides preferring high bicarbonate content (118–144.50 mg/L) with low pH values (7.63–7.97). Species composition and abundance of rotifer population in Anchar lake was carried out by Balkhi et al. [78] reporting 33 taxa. They categorized them into three groups viz; cold stenothermal (five species), eurythermal (eight species), and warm stenothermal (20 species). Among the species recorded Polyarthra vulgaris was considered to be cold stenothermal, but the same species was classified as perennial by Yousuf and Qadri [66]. In another detailed hydrobiological study of Anchar lake Balkhi et al. [71] reported 41 species of rotifers, with Asplanchna priodonta being the most dominant species in the rotifer community. Euchlanis dilatata, Proalinopsis sp. and Trichotria tetractis were categorized into eurythermal, while the species like Lecane sp. Monostyla sp. and Mytilina mucronata form warm stenotherms, whereas Notholca acuminata, Colurella sp. and Trichocerca cylindrica were the chief cold stenotherms in the lake. In still another study, Yousuf and Qadri [79] while studying distribution of Polyarthra vulgaris Carlin acclaimed the species to be a perennial, eurythermal (tolerating wide range of temperature 5.6–28.90 °C) and attaining only single peak of population (late winter). Distribution of the same species is controlled by a number of abiotic factors such as increase in temperature, pH, carbonates etc. besides some biotic factors especially for Diaphanosoma brachyurum, a cladoceran, that probably competes with the food of Polyarthra vulgaris. Pandit [80] while studying the plankton dynamics in freshwater wetlands of Kashmir (Nowgam, Malgam, Hiagam, Mirgund and Hokarsar] opined that 70–80 % of the rotifer community was constituted by eurythermal species (Keratella sp., Brachionus sp., Lecane sp., Monostyla lunaris, Filina opliensis, Cephalodella sp., Trichocera sp. and Synchaeta pectinata) while less frequent species (Platyias sp. and Diplois sp) were warm stenothermal organisms. Other species, which showed sporadic distribution and prefering cold to moderate temperatures, were Pompholyx sp., Colurella bicuspidata, Monostyla bulla, Notholca acuminata, Gastropus stylifer, Euchlanis diliata, Epiphanes sp. and Polyarthra vulgaris.

Food and Feeding Habits

Feeding ecology of zooplankton is necessary to understand the pelagic trophic dynamics in aquatic systems [80, 81]. In Kashmir Himalaya detailed studies have been carried out by Pandit and Kaul [82] and Pandit [4, 83] on the trophic structure of some typical wetlands in general and plankton community in particular, drawing attention towards the inter-relationships between the phyto- and zooplankton. All these studies basically focus on the various food and feeding habits of zooplankton as delineated in various food chains and food webs. Rotifers according to the authors have been categorized into herbivores (Polyarthra vulgaris, Epiphanes sp., Keratella cochlearis and Trichocera sp. with the last two species were often seen drilling into an algal filament to suck out its contents), Euchlanis diliata as omnivore and feeding on Pandorina, diatoms and protozoans, and Asplanchna priodonta, Syncheata sp., Pectinata sp., and Gastropus stylifer as raptorial predators (former rotifer shows preference for Brachionus sp. over other available rotifers). Brachionus sp., Keratella valga, K.quadrata, Monostyla sp., Lecane sp., Notholca acuminata, Philiodina sp., Colurella sp., Platyias sp., Diplois sp., Mytilina sp., Pompholyx sp. and Filina sp. were categorized as secondary consumers. They further opined that Keratella cochlearis, B. calyciflorus, Epiphanes sp. and Asplanchna priodonta as pollution tolerant species.

Vertical Migration

Diel vertical migration (DVM) by zooplankton is a universal feature and well studied behavior in all the freshwater bodies probably represents the biggest animal migration, in terms of biomass, on the planet [84–87]. Till date only two published reports were available regarding the vertical migration of rotifers in Kashmir Himalaya. Khan [70] while studying periodicity of zooplankton in two flood plain lakes (Trigamasar and Naranbagh] inferred that there was a clear periodicity among the rotifers between the upper and bottom layers and showed four times denser population (5,400 units/L) in bottom layers than the surface layer (1,375 units/L) of Trigamasar. Yousuf and Mir [60] while studying the vertical distribution in a warm monomictic Manasbal lake of Kashmir recorded 23 species of rotifers from the limnetic zone having trimodal pattern of fluctuations with two distinct peaks in late March and August and the third, a feeble, one in the month of May. They further opined thermal stratification being one of the main causes, besides vertical distribution of gases and nutrients, responsible for the distribution patterns of these animals. The recorded species showed different behaviour in response to thermal stratification. For example Polyarthra vulgaris and Keratella cochlearis, (former being the most dominant species) both prefer metalimnion with perennial behaviour.

Conclusion

In conclusion, the research on rotifers, making an important component of zooplankton community, needs further detailed exploration in a vast spectrum of freshwater bodies of Kashmir including lakes, wetlands, springs and streams, though scanty and inconsistent information is available on taxonomy, species composition and density of the wheel animalcules. Detailed taxonomic survey based on the species morphology using very recent approaches like SEM techniques and DNA bar coding is the much needed research enabling the limnologists to make a correct and exhaustive identification of the species. The role of the rotifers as biomonitoring tools and an important food source in the aquatic food chains are also other important aspects of the ecology of rotifers.