Journal of Threatened Taxa | www.threatenedtaxa.org | 26 August 2024 | 16(8): 25700–25711

 

ISSN 0974-7907 (Online) | ISSN 0974-7893 (Print) 

https://doi.org/10.11609/jott.8971.16.8.25700-25711

#8971 | Received 15 February 2024 | Final received 28 June 2024 | Finally accepted 16 August 2024

 

 

The present state of leech fauna (Annelida: Hirudinea) in Dal Lake, Jammu & Kashmir, India

 

Niyaz Ali Khan 1 , Zahoor Ahmad Mir 2 & Yahya Bakhtiyar 3

 

1,2,3 Fish Biology and Limnology Research Laboratory, Department of Zoology, University of Kashmir, Srinagar, Jammu & Kashmir 190006, India.

 1 niyazali411@gmail.com, 2 mirzahoor88@gmail.com, 3 yahya.bakhtiyar@gmail.com (corresponding author)

 

 

Editor: Chandra Kanta Mandal, Zoological Survey of India, Kolkata, India.               Date of publication: 26 August 2024 (online & print)

 

Citation: Khan, N.A., Z.A. Mir & Y. Bakhtiyar (2024). The present state of leech fauna (Annelida: Hirudinea) in Dal Lake, Jammu & Kashmir, India. Journal of Threatened Taxa 16(8): 25700–25711. https://doi.org/10.11609/jott.8971.16.8.25700-25711

  

Copyright: © Khan et al. 2024. Creative Commons Attribution 4.0 International License. JoTT allows unrestricted use, reproduction, and distribution of this article in any medium by providing adequate credit to the author(s) and the source of publication.

 

Funding: One of the authors Niyaz Ali Khan is highly thankful to the Council of Scientific and Industrial Research (CSIR) for providing financial assistance in the form of SRF CSIR sanction letter no.09/251(0160)/2019-EMR-I

 

Competing interests: The authors declare no competing interests.

 

Author details: Niyaz Ali Khan Ph.D. research scholar, Department of Zoology, University of Kashmir is currently working in the Fish Biology and Limnology Research Laboratory on the taxonomy of aquatic annelids. Zahoor Ahmad Mir Ph.D. in zoology working on the taxonomy and ecology of macrobenthic invertebrates. Yahya Bakhtiyar Ph.D. in zoology currently working as senior assistant professor in the Department of Zoology, University of Kashmir, supervises the team in Fish Biology and Limnology Research Laboratory on broad research areas like fish population dynamics, reproductive biology, zooplankton, macrobenthic invertebrates, and limnology with reference to Kashmir Himalaya.

 

Author contributions:  Conceptualization—Yahya Bakhtiyar, Niyaz Ali Khan. Methodology—Niyaz Ali Khan, Zahoor Ahmad Mir. Identification—Niyaz Ali Khan, Yahya Bakhtiyar, Zahoor Ahmad Mir. Writing—original draft preparation—Niyaz Ali Khan, Yahya Bakhtiyar. Review and editing— Yahya Bakhtiyar, Niyaz Ali Khan, Zahoor Ahmad Mir. Supervision—Yahya Bakhtiyar.

 

Acknowledgements:The authors are highly thankful to the head of the Department of Zoology, University of Kashmir for providing the necessary facilities while conducting this research work.

 

 

Abstract: Dal Lake supports a diverse group of fauna, including fishes, aquatic birds, zooplankton, and macrobenthic invertebrates. This study is the first taxonomic documentation of the leech fauna of Dal Lake. A total of nine leech taxa belonging to four families were identified and described: Glossiphoniidae – Alboglossiphonia weberi, A. heteroclita, Glossiphonia complanata, Helobdella stagnalis, Hemiclepsis marginata asiatica, and Theromyzon sp.; Erpobdellidae – Erpobdella octoculata; Hirudinidae – Poecilobdella granulosa; and Haemopidae – Haemopis indicus. Leeches play key roles in prey-predator dynamics and host-parasite relationships in freshwater ecosystems and as bioindicators of water pollution. This study provides essential data for taxonomic accounts and the diversity of leech fauna in Dal Lake.

 

Keywords: Freshwater ecosystem, annelid diversity, Himalaya, taxonomy, distribution, Glossiphoniidae, Erpobdellidae, Hirudinidae, Haemopidae.

 

 

INTRODUCTION

 

Leeches are annelids that coexist in freshwater ecosystems with molluscs, oligochaetes, and insect larvae and are found on every continent and in every ocean, except for terrestrial Antarctica (Sket & Trontelj 2008). Leeches prefer diverse environments and exhibit tolerance to extreme conditions such as variation in temperature, moisture, salinity, pressure, light, and pollution. They can be found in some wet soil on land and bottom substrates of freshwater, estuarine, and marine ecosystems (Phillips et al. 2020). Leeches are regarded as one of the most significant ecological indicators in freshwater ecosystems. Several aquatic species of leeches are important components in the aquatic food web at different trophic levels and also play a role in prey-predator and parasite-host relationships. Additionally, they are good bioindicators of water pollution, making them highly relevant from a scientific perspective (Bezmaternykh 2007; Romanova & Klimina 2010; Kaygorodova et al. 2014). Leeches serve as intermediary hosts for some larval stages of trematodes and are essential components of prey-predator and parasite-host relationships in aquatic environments (Pyrka et al. 2021). Around one-third of the total leech species have feeding mode as predators, while majority of leech species consume the blood of other invertebrates and vertebrates for their nutrition (Atkauskien & Rutkauskaitė-Sucilien 2022). Considering the taxonomic accounts, leeches have a circumoral and a posterior ventral sucker for attachment to substratum as well as a fixed number of segments (Wetzel 1992). They also lack setae but have a genital orifice and analogue jaws as diagnostic characters. One of the species, Hirudo medicinalis, of the class Hirudinea was traditionally used to treat people suffering from a variety of illnesses and medical ailments (Sig et al. 2017). In India, numerous new species of terrestrial and freshwater leeches have been documented over time beginning with the works of (Harding 1924; Baugh 1960 a,b; Soota & Ghosh 1977; Chandra 1982; Nesemann et al. 2004; Mandal 2004, 2013, 2015; Mandal et al. 2020a,b, 2022; Uttam & Langer 2021). There is a significant lack of comprehensive data regarding the distribution, biology, and ecology of many Indian leech species (Bhatia 1930, 1940; Baugh 1960 a,b; Ray 1980; Raut & Nandi 1985; Raut 1986; Raut & Saha 1987; Mandal et al. 2022). The existing literature regarding the leech fauna in the Kashmir valley’s water bodies is mostly fragmented. Moreover, there are very few old records about the species composition of leeches from the waterbodies of Kashmir. In the 20th century, Moore (1924); Bhatia (1930, 1934, 1939, 1940), and Soota (1956) conducted studies on the leech fauna in Kashmir. Therefore, the literature reveals the need for fresh surveys and redescription of species regarding the leech fauna in freshwater bodies of the Kashmir valley. Considering the taxonomic concerns and lack of data available regarding the leech fauna, the present study has been conducted to explore the current leech fauna of Dal Lake.

 

 

MATERIALS AND METHODS

 

Study area

Dal Lake, one of the most cherished water bodies, in the Kashmir Himalaya, is situated in the urban area, providing numerous ecosystem services to the local population and boosting the urban economy. The lake is located between geographic coordinates 34.067–34.183 °N & 74.800–74.880 °E (Figure 1) covering a total catchment area of approximately 337 km2. The lake has a surface area of 24 km2, with 10.5 km2 available as open water (Rashid et al. 2017). It is divided into four distinct basins: Hazratbal, Lokut Dal, Nigeen, and Gagribal (Amin et al. 2014). Dal Lake functions as an open drainage system, receiving water input from various streams and springs. Telbal Nallah and Botkol serve as the two main inflow channels, while smaller streams such as Meerakshah Nallah along with multiple springs originating from the lake bed and nearby mountains contribute to its water sources (Qadri & Yousuf 1980). The lake has two primary outlets, namely Nallah Amir Khan and Dalgate (Kumar et al. 2022). In the present study, the samples were collected from different locations within Dal Lake.

 

Methods applied for sampling, processing, and identification

Freshwater leeches were collected with standard bottom samplers (EU-WFD) used in different zones of Dal Lake, during the research work from January 2021 to December 2022. An Ekman’s dredge was used to collect the mud samples in the deep water (limnetic zone) while the kick method was applied in shallow water (littoral zone) to collect samples from macrophytes, leaf packs, submerged logs, stones, concrete banks, and debris. Leech samples were carefully separated from extraneous material by handpicking tools and delivered as live samples in water- filled plastic jars (1l) to the Fish Biology and Limnology Research Laboratory, Department of Zoology, University of Kashmir. The specimens were first narcotized using a gradient of low ethanol solutions and then preserved in 80% ethanol following the standard protocol of Kaygorodova & Bolbat (2020). Morphological analysis and photography were carried out using stereo zoom microscopes (Magnus MS 24 and LEICA S98) with a digital microscope camera (Magcam DC 10). Identification of species was done by using existing standard taxonomic keys of leeches (Klemm 1985; Chandra 1991; Nesemann et al. 2004; Mandal 2013).

 

 

RESULTS AND DISCUSSION

 

Family: Glossiphoniidae

Alboglossiphonia weberi (Linnaeus, 1761)

Location: Telbal, 34.140oN & 74.863oE, 29.viii.2021, 13.ix.2022, coll. Niyaz Ali Khan.

Material examined: Image 1A–C; number of specimens observed = 15.

Diagnosis: The body is translucent ovate 10 mm in length; the dorsal surface is roughened by the presence of numerous tubercles (Image 1A); colour of the live specimen is somewhat yellowish-brown and on preservation in alcohol it becomes greenish white; it possesses a radial stripe of the same dark pigment which occurs upon the body (Image 1A); Presence of three pair of eyes one each on sixth, seventh and eighth ring (Image 1C); crop with six pairs of lateral diverticula.

Habitat: Alboglossiphonia weberi occurs in ponds, tanks, pools, lakes, slow-moving streams, and rivers. This species is found attached to the smooth surfaces of cobbles and pebbles in streams, and rivers.

Distribution: Widely distributed throughout India while outside India occurs in Pakistan, Nepal, Myanmar, and Sumatra (Chandra 1991).

 

Glossiphonia complanata (Linnaeus, 1758)

Location: Telbal, 34.140oN & 74.863oE, 27.viii.2021, 15.iii.2022, coll. Niyaz Ali Khan; Nigeen, 34.123oN & 74.827oE, 27.viii.2021, coll. Niyaz Ali Khan; Ashai bagh, 34.114oN & 74.836oE, 27.viii.2021, 15.iii.2022, coll. Niyaz Ali Khan.

Material examined: Image 1D–H; n = 23.

Diagnosis: Body flat, leaf- shaped, dark brown and greenish in colour; the length is 14–25 mm; dorsal surface of the body is covered with six rows of papillae; dorsal surface has two paramedial dark lines interrupted by papilla which extends up to the middle portion of the body (Image 1D,G); two strips are also prominent on the ventral side (Image 1E); three pair of eye spots located on the anterior somite’s (Image 1F); posterior sucker is disk- like while the anterior sucker is triangular; six pair of crop caeca can be seen in freshly collected live specimens.

Habitat: Glossiphonia complanata was commonly found in stagnant water bodies and slow-flowing rivers characterized by plentiful vegetation and molluscs. Typically, this species was observed under submerged wood or stones.

Distribution: The species is widely distributed in India such as Jammu & Kashmir, Himachal Pradesh, Uttar Pradesh, Rajasthan, Maharashtra, Karnataka, Madhya Pradesh, Bihar, West Bengal, Meghalaya, Manipur, and Odisha while outside India it has been reported from Pakistan, Nepal, Myanmar, Indonesia, Japan, U.S.A, and Europe (Chandra 1991; Mir et al. 2024).

 

Alboglossiphonia heteroclita (Linnaeus, 1761)

Location: Telbal, 34.140oN & 74.863oE, 29.iii.2021, coll. Niyaz Ali Khan; Nigeen, 34.123oN & 74.827oE, 10.viii.2021, coll. Niyaz Ali Khan.

Material examined: Image 2A–C; n = 23.

Diagnosis: Small, flat, and ovate leeches are generally yellowish translucent in live specimens; the head region is bulbous consisting of three pair of eyes of which the first pair of eyes lie close to each other and are the smallest ones as compared to the other two pairs (Image 2C); second and third pair of eyes are widely separated but the components lie near together giving approximately a triangular shape (Image 2C); three pair of eyes generally lie in rings five , seven and eight respectively; one median line of dark black spots on every third annulus and numerous small spots on the dorsal surface (Image 2A); dorsal and ventral surface of the body is smooth and without papillae (Image 2A,B).

Habitat: Alboglossiphonia heteroclita is found in lakes and ponds attached to submerged articles and are parasitic mainly on molluscs (Chandra 1991).

Distribution: Alboglossiphonia heteroclita is a species with a Holarctic distribution, found in central and western Europe (Nesemann & Neubert 1999; Bielecki et al. 2011). It has also been recorded in Lithuania while in India, the species occur in Rajasthan and Bihar (Chandra 1991).

 

Helobdella stagnalis (Linnaeus, 1758)

Location: Telbal, 34.140oN & 74.863oE, 2.iv.2021, 22.x.2022, coll. Niyaz Ali Khan.

Material examined: Image 3A–C; n = 7.

Diagnosis: Small flat, leaf- shaped ceramic white when alive and pale white on preservation with numerous tiny spots on the dorsal surface; an anterior region with a single pair of eyespots and a chitinous scute (nuchal plate) is visible on the dorsum (Image 3A,C); smooth body surface without any papillae.

Habitat: Helobdella stagnalis is found in stagnant water bodies in association with molluscs. Adults show parental care where young ones are attached to the ventral side of the body (Image 3B).

Distribution: In India, the species occur in Himachal Pradesh and Jammu & Kashmir (Mir et al. 2024) while outside India it has been reported from the USA, Lithuania (Zettler & Daunys 2007), Canada, and Paraguay (Chandra 1991).

 

Theromyzon sp. Philippi, 1867

Location: Telbal, 34.140oN & 74.863oE, 22.x.2021, coll. Niyaz Ali Khan.

Material examined: Image 3D– J; n = 33.

Diagnosis: Large dorsoventrally flattened olive green or brownish in colour (Image 3G); preserved specimens are brownish due to decolouration (Image 3D); six rows of yellow spots on the dorsal side of the body; ventral side possesses a large number of small papillae; suckers are small and weak in comparisons to the body size; four pair of eyespots arranged straight in head region; first pair of eyespots lie close to each other and second, third and fourth pair of eyes widely separated in ascending order (Image 3J); four annuli between male and female gonopore (Image 3F); young ones appear green in colour and are found attached to the ventral side of the parent body (Image 3H).

Habitat: Theromyzon sp. was found mainly in the stagnant water with the presence of aquatic birds. They are found attached to the submerged articles, under stones and wood. Adult shows parental care where around 100 young ones are attached to the ventral side of the body (Image 3H).

Distribution: Theromyzon sp. has been reported in many states of India (Chandra 1982) while outside India, the species occurs in European, American, and African countries (Davies et al. 2008).

 

Hemiclepsis marginata asiatica (Moore, 1924)

Location: Telbal, 34.140oN & 74.863oE, 27.viii. 2021, coll. Niyaz Ali Khan.

Material examined: Image 4A–D; n = 11.

Diagnosis: The leech is commonly known as the disproportioned- eyed leech; two pairs of eyes are present, with the anterior pair being extremely small (Image 4C); the first pair of eyes are closely positioned and very tiny (Image 4C); eyes are typically located just ahead of the more noticeable and widely spaced posterior pair of eyes; leech is translucent in appearance; size is approximately 16 mm in length and 6 mm in width; the head region is enlarged and differentiated from the rest of the body; leech exhibits a reddish-brown colour in natural environment and whitish on preservation; dorsal surface with broken transverse stripes in a pale-yellow (Image 4A); crop region contains 11 pairs of lateral diverticula.

Habitat: Hemiclepsis marginata asiatica is common in shallow margins of lakes and ponds overgrown by vegetation. Found attached to submerged articles, plants, stones, and wood as microhabitats.

Distribution: Mostly occurs in Jammu & Kashmir and Himachal Pradesh states of India (Chandra 1991; Mir et al. 2024).

 

Family: Erpobdellidae

Erpobdella octoculata (Linnaeus, 1758)

Location: Telbal, 34.140oN & 74.863oE, 2.i.2021, coll. Niyaz Ali Khan; Nigeen, 34.123oN & 74.827oE, 2.i.2021, coll. Niyaz Ali Khan; Ashai bagh, 34.114oN & 74.836oE, 17.viii.2021, 27.viii.2022, coll. Niyaz Ali Khan.

Material examined: Image 4E–H; n = 43.

Diagnosis: These leeches vary in size, ranging from medium to large, and also exhibit a variety of colours; possess a relatively robust body form compared to other species in the same family, with a nearly uniform shape that tapers anteriorly to the clitellum; head is relatively small in proportion (Image 4E); typically, they have four pairs of eyes; first pair located on segment II; second pair at the furrow between segments II and III; third and fourth pairs situated on the sides of the buccal ring on segment IV (Image 4F); breeding individuals display a well-defined clitellum; gonopores are separated by approximately two and a half annuli (Image 4H).

Habitat: Most common leech species found in both lentic and lotic water bodies attached to stones, submerged articles, and leaves of aquatic plants.

Distribution: In India, occurs mostly in Jammu and Kashmir (Mir et al. 2024) while outside India, it occurs in Lahore (Pakistan), Palestine, and Europe (Chandra 1991).

 

Family: Hirudinidae

Poecilobdella granulosa (Savigny, 1826)

Location: Nigeen, 34.123oN & 74.827oE, 10.ix.2021, coll. Niyaz Ali Khan.

Material examined: Image 5(A–D); n = 10.

Diagnosis: The average adult body is about 70 mm long; dark greenish-brown in colour, and has a dorsal surface covered in geometrically structured black patterns and squares (Image 5A); the median line is always dark; the body is solid and has a very rough surface with the abundance of big papillae; typical five sets of eyes present (Image 5C).

Habitat: Poecilobdella granulosa was found in stagnant water or nearly stagnant water bodies with muddy bottoms, vegetation, and water with organic- rich material.

Distribution: In India, occurs in Punjab, Himachal Pradesh, Uttar Pradesh, Gujrat, Maharashtra, Madhya Pradesh, Tamil Nadu (Chandra 1983), Jammu & Kashmir, Kerala, Manipur, Odisha, Rajasthan, Sikkim, Uttarakhand, and West Bengal (Ahmed 2021) while outside India, occurs in Sri Lanka, Nepal, and Myanmar.

 

Family: Haemopidae

Haemopis indicus Bhatia, 1940

Location: Ashai Bagh, 34.114oN & 74.836oE, 3.iii.2022, coll. Niyaz Ali Khan.

Material examined: Image 6A–C; n = 6.

Diagnosis: The body of the leech is characterized by its remarkably soft and flabby texture; it appears thick for the majority of its length; gradually tapering towards both ends; the ventral surface is relatively flat; the dorsal surface is broadly arched; the posterior sucker is small and lacks strength; leech displays a dark colouration without any distinct markings (Image 6A); the arrangement of the five pairs of eyes follows the typical pattern; fourth eye separated from the third by a single annulus; fifth eye separated from the fourth by two annuli; gonopores are separated by approximately five and a half annuli (Image 6B).

Habitat: Haemopis indicus also known as barrowing leech was mainly found attached to submerged articles in stagnant water bodies or nearly stagnant water rich in organic matter and vegetation.

Distribution: The species has been mostly reported in Jammu and Kashmir, India (Chandra 1991; Mir et al. 2024).

During the present study, a total of nine taxa belonging to the class Hirudinea were identified on the basis of morphological characteristics like colour, size and shape, number and position of eyes, papillation, number of annulations, and position of male and female gonopores (Table 1). The taxa identified were Alboglossiphonia weberi, A. heteroclita, Glossiphonia complanata, Helobdella stagnalis, Hemiclepsis marginata asiatica, Theromyzon sp., Erpobdella octoculata, Poecilobdella granulosa, and Haemopis indicus. As per earlier record, Bhatia (1939) described and reported Theromyzon mathai from Kashmir which is morphologically similar to Theromyzon sp. collected during the current study except the latter possesses four annuli between male and female gonopore instead of three annuli. The collected specimen resembles more to the European species Theromyzon tessulatum but it still needs confirmation based on the comparative studies with the closer species of Theromyzon sp. The paper presents the first photographic documentation of aquatic leeches occurring in Dal Lake. This study redescribed the leech species that were previously recorded in the valley. In contrast to the previous species found in the valley, most of the species are found in Dal Lake and many other species have no records. Based on existing records, there have been a total of 32 known leech species documented in Jammu and Kashmir (Mandal et al. 2022). To verify the species richness and specifically identify any new species, it is necessary to conduct proper surveys in the water bodies of the valley to overcome the fragmented and scanty record of the previous two decades. The current knowledge of leech diversity in Kashmir is far from being a comprehensive study and needs detailed surveys for complete documentation.

 

 

CONCLUSION

 

The present study provides knowledge about the taxonomic description, habitat, and distribution of freshwater leech fauna from the Kashmir Himalaya. A total of nine species belonging to four families of class Hirudinea were recorded and documented. Six species were reported from the family Glossiphonidae while single species were reported each from the families Hirudinidae, Erpodellidae, and Haemopidae. As per the literature and present status, the habitat of leech fauna has been disturbed due to growing poor water quality and shrinkage of freshwater water bodies. The present study has been conducted to address the taxonomic record of leech fauna in Dal Lake of Kashmir Himalaya.

 

 

Table 1. The systematic list of leech species collected from Dal Lake.

Phylum

Class

Order

Family

Genus/Species

Authority

Common Name

Annelida

 

Hirudinea

 

 

 

Rhynchobdellida

 

Glossiphoniidae 

Alboglossiphonia weberi

(Blanchard, 1897)

Proboscis-bearing Leech

Glossiphonia complanata

(Linnaeus, 1758)

Proboscis-bearing Leech

Helobdella stagnalis

(Linnaeus, 1758)

Proboscis-bearing Leech

Theromyzon sp.

Philippi, 1867

Duck Leech

Alboglossiphonia hetroclita

(Linnaeus, 1761)

Small Snail Leech

Hemiclepsis marginata asiatica

(Moore, 1924)

Disproportioned-eyed leech

 Archynchobdellida

Erpobdellidae

Erpobdella octoculata

(Linnaeus, 1758)

Worm Leech

Hirudinidae

Poecilobdella granulosa

(Savigny, 1826)

Cattle Leech

Haemopidae

Haemopis indicus

(Bhatia, 1940)

Blood-sucking Leech

 

 

For images - - click here for full PDF

 

 

REFERENCES

 

Ahmed, S. (2021). Annelida: Hirudinea (Leeches). Zoological Survey of India, Fauna of Himachal Pradesh, State Fauna Series 26: 51–56.

Amin, A., S. Fazal, A. Mujtaba & S.K. Singh (2014). Effects of land transformation on water quality of Dal Lake, Srinagar, India. Journal of the Indian Society of Remote Sensing 42: 119–128. https://doi.org/10.1007/s12524-013-0297-9

Atkauskien, I. & J. Rutkauskait-Sucilien (2022). The present state of the leech fauna (Annelida: Hirudinea) in Lithuania. Zootaxa 5115(1): 47–62. https://doi.org/10.11646/zootaxa.5115.1.3

Bandyopadhyay, P.K. & C.K. Mandal (2006). Studies on a new species of leech of the genus Haemadipsa (Hirudinea: Haemadipsidae) from the Kodair forest of Tamil Nadu, India. Records of the Zoological Survey of India 106(1): 33–37. https://doi.org/10.26515/rzsi/v106/i1/2006/159213

Baugh, S.C. (1960a). Studies on Indian Rhynchobdellid leeches. I. Parasitology 50(3–4): 287–301. https://doi.org/10.1017/s0031182000025403

Baugh, S.C. (1960b). Studies on Indian Rhynchobdcllid leeches. II. Zoologischer Anzeiger 165: 468–477.

Bezmaternykh, D.M. (2007). Zoobenthos as an indicator of water ecosystems state in Western Siberia. Ecology, A series of Analytical Reviews of World Literature 85: 1–86.

Bhatia, M.L. (1930). Sur une nouvelle hirudinée rhynchobdelle, Glossiphonia cruciate n. sp., provenant du vivier à truites d’Achha Bal, Kashmir. Annales de Parasitologie Humaine et Comparée 8(3-4): 344–348. https://doi.org/10.1051/parasite/1930083344

Bhatia, M.L. (1934). Nouvelle sangsu rhynchobdellide Glossiphonia lobata n. sp. de l’établishment de pisciculture d’Achha Bal (Kashmir). Annales de Parasitologie Humaine et Comparée 12(2): 121–129. https://doi.org/10.1051/parasite/1934122121

Bhatia, M.L. (1939). On some leeches from Kashmir. Bulletin of Punjab University Zoology 2: 1–17.

Bhatia, M.L. (1940). On Haemopis indicus n. sp. a new Arhynchobdellid carnivorous leech from Kashmir. Proceedings of the National Academy of Sciences, India. Section B 10(4): 133–144.

Bielecki, A., J.M. Cichocka, I. Jeleń, P. Świątek & Z. Adamiak-Brud (2011). A checklist of leech species from Poland. Wiadomości Parazytologiczne 57(1): 11–20.

Chandra, M. (1982). A check-list of leeches of India. Records of the Zoological Survey of India 80: 265–290.

Chandra, M. (1983). The leech fauna of the Jammu region of Jammu and Kashmir state, India. Records of the Zoological Survey of India 81(1–2): 289–298. https://doi.org/10.26515/rzsi/v81/i1-2/1983/161269

Chandra, M. (1991). The Leeches of India. Zoological Survey of India, Calcutta 3782: 1–17.

Davies, R.W., F.R. Govedich & W.E. Moser (2008). Leech parasites of birds, pp 501–511. In: Atkinson, C.T., N.J. Thomas, D.B. Hunter (eds.). Parasitic Diseases of Wild Birds. John Wiley & Son, 595 pp. https://doi.org/10.1002/9780813804620.ch28

Harding, W.A. (1924). Descriptions of some new Leeches from India, Burma, and Ceylon. Annals and Magazine of Natural History 14(82): 489–499. https://doi.org/10.1080/00222932408633143

Kaygorodova, I., N. Bolbat & A. Bolbat (2020). Species delimitation through DNA barcoding of freshwater leeches of the Glossiphonia genus (Hirudinea: Glossiphoniidae) from Eastern Siberia, Russia. Journal of Zoological Systematics and Evolutionary Research 58(4): 1437–1446. https://doi.org/10.1111/jzs.12385

Kaygorodova, I.A., N. Mandzyak, E. Petryaeva & N.M. Pronin (2014). Genetic diversity of freshwater leeches in lake gusinoe (Eastern Siberia, Russia). The Scientific World Journal 2014: 1–11. https://doi.org/10.1155/2014/619127

Klemm, D.J. (1985). A guide to the Freshwater Annelida (Polychaeta, Naidid and Tubificid Oligochaeta, and Hirudinea) of North America. Kendall Hunt Publishing Company, Dubuque, Iowa, 198 pp.

Kumar, R., S. Parvaze, M.B. Huda & S.P. Allaie (2022). The changing water quality of lakes - a case study of Dal Lake, Kashmir Valley. Environmental Monitoring and Assessment 194(3): 228. https://doi.org/10.1007/s10661-022-09869-x

Mandal, C. K. (2004). Endemic leech fauna of India. Records of the Zoological Survey of India 80: 103–110. https://doi.org/10.26515/rzsi/v103/i1-2/2004/159489

Mandal, C.K. (2013). Annelida: Hirudinida: Fauna of Karnataka. Zoological Survey of India 21: 51–55.

Mandal, C.K. (2015). Paraclepsis jorapariensis sp. nov. (Hirudinea: Glossiphonidae): a new leech from Jharkhand, India. Records of the Zoological Survey of India 115(3): 231–235. https://doi.org/10.26515/rzsi/v115/i3/2015/120707

Mandal C.K., H. Tariyal, P. Naiwal, D. Thakur & S. Ghosh (2020a). Haemadipsa champhaiensis sp. nov. (Hirudinea: Hirudidae): a new leech from Mizoram, India. Journal of Applied Zoological Research 31(1): 86–90.

Mandal C.K., H. Tariyal, P. Naiwal, D. Thakur & S. Ghosh (2020b). Haemadipsa satyanarayanai sp. nov. (Clitellata: Haemadipsidae): a new leech from Nagaland, India. Journal of Applied Zoological Research 31(2): 149–155.

Mandal, C.K., J.W. Reynolds, M.N. Hasan & K. Deuti (2022). Leech fauna of north- east India (Annelida: Hirudinea). Megadrilogica 27(1): 1–12.

Mir, Z.A., Y. Bakhtiyar, M. Parveen & N.A. Khan (2024). Taxonomy and diversity of Annelids in two Jhelum tributaries of Kashmir Himalaya, India. Proceedings of National Academy of Sciences, India, Section B Biological Sciences 1–9. https://doi.org/10.1007/s40011-024-01607-2

Moore, J.P. (1924). Notes on some Asiatic leeches (Hirudinea) principally from China, Kashmir, and British India. Proceedings of the Academy of Natural Sciences of Philadelphia 76: 343–388.

Nesemann, H. & E. Neubert (1999). Annelida, Clitellata: Branchiobdellida, Acanthobdellea, Hirudinea. Süßwasserfauna von Mitteleuropa 6: 27–32.

Nesemann, H., G. Sharma & R.K. Sinha (2004). Aquatic Annelida (Polychaeta, Oligochaeta, Hirudinea) of the Ganga River and adjacent water bodies in Patna (India: Bihar), with description of a new leech species (Family Salifidae). Annalen des Naturhistorischen Museums in Wien 105(B): 139–187.

Phillips, A.J., F.R. Govedich & W.E. Moser (2020). Leeches in the extreme: morphological, physiological, and behavioral adaptations to inhospitable habitats. International Journal for Parasitology: Parasites and Wildlife 12: 318–325. https://doi.org/10.1016/j.ijppaw.2020.09.003

Pyrka, E., G. Kanarek, G. Zaleśny & J. Hildebrand (2021). Leeches as the intermediate host for strigeid trematodes: genetic diversity and taxonomy of the genera Australapatemon Sudarikov, 1959 and Cotylurus Szidat, 1928. Parasites & Vectors 14(1): 1–17. https://doi.org/10.1186/s13071-020-04538-9

Qadri, M.Y. & A.R. Yousuf (1980). Limnological studies on lake Malpur Sar 1. The Biotope Geobios 117–119.

Rashid, I., S.A. Romshoo, M. Amin, S.A. Khanday & P. Chauhan (2017). Linking human-biophysical interactions with the trophic status of Dal Lake, Kashmir Himalaya, India. Limnologica 62: 84–96. https://doi.org/10.1016/j.limno.2016.11.008

Raut, S.K. & N.C. Nandi (1985). The leech Glossiphonia weberi in the control of the snails Lymnaea luteola, a predator–prey interaction. Environment and Ecology 3(1): 21–24.

Raut, S.K. & T.C. Saha (1987). Life history of sanguivorous leech Hemiclepsis marginata marginata (Muller) Annelida: Glossiphoniidae. Indian Journal of Animal Sciences 57: 970–972.

Raut, S.K. (1986). Parental care of leech Hemiclepsis marginata marginataEnvironment and Ecology 4: 150 pp.

Ray, R. (1980). Parental care of a Glossiphonid leech, Helobdella nociva Harding. Bulletin of the Zoological Survey of India 3: 121 pp.

Romanova, E.M. & O.M. Klimina (2010). Bioresources class Hirudinea in the area of the middle Volga region: ecological significance and prospects. Proceedings of the Samara Scientific Centre of the Russian Academy of Sciences 1(12): 208–211.

Sig, A.K., M. Guney, A.U. Guclu & E. Ozmen (2017). Medicinal leech therapy — an overall perspective. Integrative Medicine Research 6(4): 337–343. https://doi.org/10.1016/j.imr.2017.08.001

Sket, B. & P. Trontelj (2008). Global diversity of leeches (Hirudinea) in freshwater. Hydrobiologia 595: 129–137. https://doi.org/10.1007/s10750-007-9010-8

Soota, T.D. & G.C. Ghosh (1977). On some Indian Leeches. Newsletter of Zoological Survey of India 3(6): 359–360.

Soota, T.D. (1956). Fauna of the Kashmir Valley: leeches. Records of the Zoological Survey of India 54(1–2): 1–4.

Uttam, S. & S. Langer (2021). Taxonomic studies and seasonal variations in density of fresh water leech Erpobdella bhatiai (Nesemann, 2007) inhabiting torrential hill stream in greater Himalayas. Indian Journal of Ecology 48(4): 1203–1208.

Wetzel, M.J. (1992). Aquatic Annelida of Illinois: introduction and checklist of species. Transactions of the Illinois State Academy of Science 85(1): 87–101.

Zettler, M.L. & D. Daunys (2007). Long-term macrozoobenthos changes in a shallow boreal lagoon: comparison of a recent biodiversity inventory with historical data. Limnologica 37(2): 170–185. https://doi.org/10.1016/j.limno.2006.12.004