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WSN 38 (2016) 1-62 EISSN 2392-2192

M O N O G R A P H

Spiders: A Proficient Candidate in Practising IPM for Darjeeling Tea

2016 World Scientific News 38 (2016) 1-62

Spiders: A Proficient Candidate in Practising IPM for Darjeeling Tea

Editors

Dinendra Raychaudhuri & Sumana Saha

Contributors

Dr. Dinendra Raychaudhuria Dr. Sumana Sahab Dr. Tapan Kumar Roy

Department of Agricultural Biotechnology, IRDM Faculty Centre, Ramakrishna Mission Vivekananda University, Narendrapur, Kolkata - 700103,

a,bE-mail address: [email protected] , [email protected]

ABSTRACT Effect of pesticides in the crop fields is now well known. Tea is no exception to this. Idea behind the present study is to appreciate the biological potential of spiders against tea pests. The study area included 6 tea estates viz. Badamtam T.E., Ging T.E., Salim Hill T.E. (organic), Castleton T.E., Namring T.E., and Thurbo T.E. (conventional). Altogether 85 species under 52 genera distributed over 18 families could be recorded. These can broadly be categorized into 7 trophic groups. The decreasing of the groups are Orb weavers (48.24%) > Ambushers (22.35%) > Ground dwellers (11.76%) ≥ Stalkers (11.76%) > Foliage hunters (9.41%) > Sheet web weavers (2.35%) > Space web builders (1.18%). Out of the total species encountered 4 species are new from the country, 2 from the state and 36 species from the study area. Based on the species richness, the decreasing order of the tea estates are BTE (61.18%) ˃ NTE (54.12%) ˃ GTE (51.76%) ˃ STE (42.35%) ˃ CTE (28.24%) ˃ TTE (25.88%). This leads to infer ‘organic tea system’ exhibits higher heterogeneity. Araneids and salticids are the dominant groups. Other than the Oriental representatives, Australian and Palaearctic are the next major groups. Nearly 32.94% of the species are found to be endemic.

Keywords: Spider fauna; diversity; tea system; Darjeeling; West Bengal; India

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ACKNOWLEDGEMENTS

Authors are indebted to Tea Board, for sponsoring the project (Sanction no. RL-33 (167)/2010/Part-VI dt.11.8.2011). All logistic support extended by the officials of the respective Tea estates, the Head, Department of Zoology, University of Calcutta and the Hon’ble Vice-Chancellor, Ramakrishna Mission Vivekananda University for carrying out the research work is thankfully acknowledged. Sincere thanks are also due to Dr. Anirban Basu Majumder, Research Officer, Tea Board for his manifold assistance. Thanks are also due to Dr. Dhruba Chandra Dhali and Dr. Sutirtha Sarkar for their cooperation during field visit.

Reviewer: Prof. Jerzy Borowski Department of Forest Protection and Ecology, Warsaw University of Life Sciences – SGGW, Warsaw, Poland

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CONTENTS 1. Introduction 5 2. Strategies Adopted 6 3. Key to symbols 7 A. New information 7 B. Guild structure 9 C. Time of activity 12 D. Abbreviations of study sites 12 E. World map showing zoogeographical regions 12 F. Time of occurrence 12 4. Spiders 13 A. Funnel web spiders: Agelenidae 13 B. Typical orb weavers: Araneidae 13 C. Sac spiders: Clubionidae 29 D. Wandering spiders: Ctenidae 30 E. Dark sac spiders: Eutichuridae 30 F. Mouse spiders: Gnaphosidae 31 G. Two tailed spiders: Hersiliidae 32 H. Sheet web spiders: Linyphiidae 32 I. Wolf spiders: Lycosidae 33 J. Long legged orb weavers: Nephilidae 36 K. Lynx spiders: Oxyopidae 37 L. Nursery web spiders: Pisauridae 39 M. Jumping spiders: Salticidae 40 N. Giant crab spiders: Sparassidae 48 O. Long jawed orb weavers: Tetragnathidae 50 P. Cobweb spiders: Theridiidae 52 Q. Crab spiders: Thomisidae 53 R. Hackled web spiders: Uloboridae 54 5. Summary 55 6. Literature Cited 56 7. Species Index 59

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1. INTRODUCTION

Spiders constitute an important component of the fauna distributed in tropical and subtropical areas of the world. Being nature’s master spinners of silken webs, they are the highly potential predators, certainly putting a check to the insect pests. Of late Entomologists/Plant Protection Specialists are laying emphasis on this tiny group as a proficient candidate of biological control. In depth knowledge on the biodiversity of spider communities of crop fields is important both in terms of enhancing pest control and understanding the driving forces influencing conservation strategies (Mansour et al., 1983; Maloney et al., 2003; Jayakumar and Sankari, 2010; Sharma, 2014) Tea, unlike other perennials, is unique because only of its vegetative parts ‘two leaves and bud’ that are commercially exploited. Cultivation practice of tea has made the monoculture ecosystem distinctive, accommodating 1031 species of and 82 species of nematodes globally (Chen and Chen, 1989; Hazarika et.al., 2009); it is 230 in Asia (Muraleedharan, 1992) while 173 arthropods and 16 nematodes are known to be pests in North-East India (Hazarika et.al., 1994). Their attack is supposed to cause yield loss to about 10-15%. India is the world’s 4th largest exporter of tea. Over the last few decades, India’s share in world tea export declined consistently for several reasons. One of the most important reasons is residual effect of pesticides in made tea. On the contrary, recent agricultural practices like organic farming towards reduced pesticide use and ecological sustainability have lead to increased interests in spiders as potential tools (Hazarika et al. 1994). The spider fauna of several crop ecosystem have been well documented in some parts of the world (Sengupta et al., 2014). In India the araneofauna of tea ecosystem are well documented by Raychaudhuri and Saha (2012), Roy (2014) and Saha and Raychaudhuri (2015). Nestling in the foothills of snow-covered Himalayan range, Darjeeling, ‘the Queen of Hills’ grows one of the world’s most exclusive teas at altitudes ranging from 300 to 2000 meters. Currently there are 87 operational tea gardens in Darjeeling district (Coordinates: 27°3ˈ N 88°16ˈ E) covering an aggregated area of about 19,000 hectares. In recent times growing appreciation and demand for the organic products has driven some tea gardens of Darjeeling to produce ‘organic tea’. But unfortunately attempt to document diversity of the spider fauna of Darjeeling tea gardens is still wanting under the changed scenario. Above prompted to study the spider species assemblage in tea ecosystem of Darjeeling, West Bengal. The study area included six tea estates namely Castleton T.E., Salim Hill T.E., Thurbo T.E. (in Kurseong Subdivision) Namring T.E. (in Kalimpong Subdivision) and Badamtam T.E. and Ging T.E. (in Darjeeling Sadar Subdivision). Among them Badamtam T.E., Ging T. E. and Salim Hill T. E. are organic gardens while Castleton T.E., Namring T.E. and Thurbo T.E. are conventional.

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Study Area

Badamtam T.E. Ging T.E.

Namring T.E. Thurbo T.E.

Castelton T.E. Salim Hill T.E.

2. STRATEGIES ADOPTED

In order to probe the state of the art, continuous monitoring on spiders was made through uninterrupted visit to the study sites during the period August, 2011 to March, 2013 in different sections of the referred tea estates. Sampling was done by visual search, hand picking, inverted umbrella, bush beating, foliage, trunk and branch scanning, pitfall and leaf litter extraction. Collected samples were preserved following Tikader (1987) and Barrion and Litsinger (1995). The collected samples were studied under Stereo Zoom Binocular Microscopes model Zeiss SV-6 & 11 and Olympus SZX7. Status of the taxa were determined with the help of Tikader (1970, 1980, 1982 & 1987), Tikader and Malhotra (1980), Majumder and Tikader (1991), Barrion and Litsinger (1995), Sebastian and Peter (2009), Keswani et al. (2012), Metzner (2015) and WSN (2015). Later they were confirmed by comparing with the type specimens deposited in Zoological Survey of India. Spider samples thus encountered are now in the deposition of Department of Agricultural Biotechnology, Ramakrishna Mission Vivekananda University.

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3. KEY TO SYMBOLS

A. New Information

New to Science

N New to India

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New to West Bengal

New to Darjeeling

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Endemic to India

B. Guild Structure

Orb weaver

Sheet web builders

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Ground dwellers

Stalkers

Foliage hunters

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Ambusher

Space web builder

C. Time of Activity

Diurnal

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Nocturnal

D. Abbreviations of study sites

BTE – Badamtam Tea Estate CTE – Castleton Tea Estate GTE – Ging Tea Estate NTE – Namring Tea Estate STE – Salim Hill Tea Estate TTE – Thurbo Tea Estate

E. World map showing zoogeographical regions

Oriental Neotropical Nearctic Australian Palaearctic Ethiopian

F. Time of occurrence

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4. SPIDERS

A. Funnel web spiders: Agelenidae

B. Typical orb weavers: Araneidae

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C. Sac spiders: Clubionidae

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D. Wandering spiders: Ctenidae

E. Dark sac spiders: Eutichuridae

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F. Mouse spiders: Gnaphosidae

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G. Two tailed spiders: Hersiliidae

H. Sheet web spiders: Linyphiidae

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I. Wolf spiders: Lycosidae

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J. Long legged orb weavers: Nephilidae

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K. Lynx spiders: Oxyopidae

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L. Nursery web spiders: Pisauridae

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M. Jumping spiders: Salticidae

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N. Giant crab spiders: Sparassidae

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O. Long jawed orb weavers: Tetragnathidae

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P. Cobweb spiders: Theridiidae

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Q. Crab spiders: Thomisidae

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R. Hackled web spiders: Uloboridae

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5. SUMMARY

The present study unfolds the spider diversity of six tea estates of Darjeeling. A total of 2072 individuals belonging to 85 morphospecies under 52 genera and 18 families are recognized. Araneids and salticids are the dominant groups. Out of 85 species four are recoded first time from the country, two from the state and thirty six species from the district Darjeeling. Twenty seven species are reported as native to India exhibiting high endemicity (32.94%). Of these, most of the species are recorded from the Araneidae (9). The generated data represents 5.04%, 11.87% and 30.0% of the Indian species, genera and family respectively. Even though species richness is little higher during premonsoon, always there remains a state of equilibrium throughout seasons. Six species viz. mitificus (Simon), Agriope pulchella Thorell, Neoscona bengalensis Tikader & Bal, Dendrolycosa gitae (Tikader), Thiana bhamoensis Thorell and decorata (Blackwall) are the dominant members and encountered in most of the months of the year. Analysis of the zoogeographical distribution reveals that the fauna apart from Oriental, includes Australian (12.94%), Palaearctic (12.94%), Ethiopian (7.05%), Nearctic (2.35%) and Neotropical (1.18%) elements. Number of recorded spider taxa from the study areas shows that species diversity is maximum in Badamtam T.E. (possesses 52 morphospecies) and minimum in Thurbo T.E. (no. of species 22). Based on species diversity, the decreasing order of the tea estates are BTE (61.18%) ˃ NTE (54.12%) ˃ GTE (51.76%) ˃ STE (42.35%) ˃ CTE (28.24%) ˃ TTE (25.88%). This leads to infer ‘organic tea system’ exhibits higher spider heterogeneity (exception in NTE). There may be two way explanation to such a fact. One may be that

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Namring T.E. being close to Teesta Valley experiences a tropical situation promoting heterogeneity or the in house species are tolerant to insecticides or both. Spiders such as Pardosa are highly tolerant to botanicals such as neem-based chemicals (Theiling and Croft, 1988; Markandeya and Divakar, 1999). They are also generally more tolerant of organophosphates and carbamates than of pyrethroids, organochlorines and various acaricides. Tolerance may due to genetic resistance bred over a period of continuous exposure (Theiling and Croft, 1988; Wisniewska and Prokopy, 1997; Yardim and Edwards, 1998; Marc et al., 1999; Tanaka et al., 2000). For example, Pardosa, Tetragnatha are highly sensitive to the inorganic chemicals, but not to botanical pesticides (Tanaka et al., 2000). Species homogeneity is more common in conventional gardens. Both diversity and density of spiders are more in organic gardens as compared to conventional ones. At any point of time diversity and density of predators are more in organic gardens. Succession of species is more in organic gardens while conventional gardens are with dominant species in more numbers. All these gardens are dominated by the members of the family Araneidae. The dominant guild is constituted by the Orb weavers (48.24%) followed by Ambushers (22.35%), Ground dwellers (11.76%) and Stalkers (11.76%), Foliage hunters (9.41%), Sheet web weavers (2.35%) and Space web builders (1.18%). The common explanation for the observed pattern of spider guilds are structural diversity, microenvironment or the level of disturbance of the habitat (Jiang and Li, 2006). Guild composition can provide insight into the effect of habitat alteration and disturbances on diversity (Stork, 1987). So, the most promising option for utilizing the predatory attributes of spiders for the biological control of pests is to increase their density and diversity within crops as physically close to pests as possible (Sunderland and Samu, 2000).

6. LITERATURE CITED

[1] Barrion, A.T. & Litsinger, J.A. 1995. Riceland Spiders of South and South East Asia. Publ. CAB International, UK & IRRI, , 716 pp. [2] Chen, Z. & Chen, X. 1989. An analysis of the world tea pest fauna. Journal of Tea Science, 9(1): 13-22. [3] Hazarika, L.K., Borthakur, M., Singh, K. & Sannigrahi, S. 1994. Present status and future prospects of biological control of tea pests in North East India. Proceedings 32nd Tocklai, Conference TRA, Tocklai Experimental Station Jorhat: 169-177. [4] Hazarika, L. K., Bhuyan, M. & Hazarika, B.N. 2009. Insect pests of tea and their management. Annual Review of Entomology, 54: 267- 284. [5] Jayakumar. S. & Sankari, A. 2010. Spider population and their predatory efficiency in different rice establishment techniques in Aduthurai, Tamil Nadu. Journal of Biopesticides, 3(1 Special Issue): 20-27. [6] Jiang, S. L. & Li, B. P. 2006. Composition and distribution of soil spider assemblages in three natural secondary forests in Ziwuling, Gansu. Zoological Research, 27(6): 569- 574.

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[7] Keswani, S., Hadole, P. & Rajoria, A. 2012. Checklist of Spiders (Arachnida: Araneae) from India-2012. Indian Journal of , 1(1): 129. [8] Majumder, S. C. & Tikader, B. K. 1991. Studies on some spiders of the family Clubionidae from India. Record Zoological Survey of India, Occasional Paper, 102: 175pp. [9] Maloney, D., Drummond, F.A. & Alford, R. 2003. Spider predation in Agroecosystems: Can spiders effectively control pest populations? Mississippi Agricultural and Forests Experimental Station Technical Bulletin, 190: 1-32. [10] Mansour, F., Richman, D.B. & Whitcomb, W.H. 1983. Spider management in agroecosystems: Habitat manipulation. Environmental Management, 7(1): 43-49. [11] Marc, P., Canard, A. & Ysnel, F. 1999. Spiders (Araneae) useful for pest limitation and bioindication. Agriculture, Ecosystems & Environment, 74: 229-273. [12] Markandeya, V. & Divakar, B.J. 1999. Effect of a neem formulation on four bioagents. Plant Protection Bulletin, 51: 28-29. [13] Metzner, H. 2015. Jumping spiders (Arachnida: Araneae: Salticidae) of the world. Online at: www.jumping-spiders.com (accessed on 25.11.2015) [14] Muraleedharan, N. 1992. Pest control in Asia. Tea cultivation to consumption. Publ. Chapman and Hall, London, 375-411. [15] Raychaudhuri, D. & Saha, S. 2012. Spiders – A potential component in tea pest management. Publ. National Tea Research Foundation, Tea Board, Kolkata, 93 pp. [16] Roy T. K. 2014. Spiders (Araneae: Arachnida) of Tea Ecosystem of Dooars, West Bengal. Ph. D. Thesis, University of Calcutta: 488 pp. [17] Saha, S. & Raychaudhuri, D. 2015. Spiders (Araneae: Arachnida) of Tea ecosystem of Assam. Publ. LAP Lambert Academic Publishing, Germany, 174 pp. [18] Sharma, S. 2014. A study on spiders as predators in the agro ecosystems. Munis Entomology & Zoology, (1): 80-83. [19] Sebastian, P. A. & Peter, K.V. 2009. Spiders of India. Publ. Universities Press (India) Pvt. Ltd., 614pp. [20] Sengupta, A., Saha, S. & Raychaudhuri, D. 2014. Diversity of spiders in different low lying crop fields of south 24-parganas, West Bengal. Indian Journal of Arachnology, 3(2): 17-27. [21] Stork, N. E. 1987. Guild structure of arthropods from Bomean rain forests trees. Ecological Entomology, 12: 69-80. [22] Sunderland, K. & Samu, F. 2000. Effects of agricultural diversification on the abundance, distribution, and pest control potential of spiders: A review. Entomologia Experimentalis et Applicata, 95: 1-13. [23] Tanaka, K., Endo, S. & Kazano, H. 2000. Toxicity of insecticides to predators of rice planthoppers, spiders, the mirid bug and the dryinid wasp. Applied Entomology & Zoology, 35: 177-187.

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[24] Theiling, K. M. & Croft, B. A. 1988. Pesticide side-effects on arthropod natural enemies: A database summary. Agriculture, Ecosystems & Environment, 21: 191-218. [25] Tikader, B.K. 1970, The spider fauna of Sikkim Himalaya India. Record Zoological Survey of India, 64(14): 1-84. [26] Tikader, B.K. 1980. The Fauna of India, Araneae: Thomisidae (crab spiders). Zoological Survey of India, Calcutta, I(1): 1-247. [27] Tikader, B.K. 1982. The Fauna of India, Spider: Araneae (Araneidae & Gnaphosidae). Zoological Survey of India, Calcutta, II(1): 533 pp. [28] Tikader, B.K. 1987. Hand book of Indian spiders. Ed. Director Zoological Survey of India, Calcutta: 251 pp. [29] Tikader, B.K. & Malhotra, M.S. 1980. Fauna of India, spiders (Lycosidae). Zoological Survey of India, Calcutta, I(2): 248-447. [30] Wisniewska, J. & Prokopy, R.J. 1997. Pesticide effect on faunal composition, abundance, and body length of spiders (Araneae) in apple orchards. Environmental Entomology, 26: 763-776. [31] World Spider Catalog. 2015. World Spider Catalog. Natural History Museum Bern, online at http://wsc.nmbe.ch, version 16.5 (accessed on 25.11.2015). [32] Yardim, E.N. & Edwards, C.A. 1998. The influence of chemical management of pests, diseases and weeds on pest and predatory arthropods associated with tomatoes. Agriculture, Ecosystems & Environment, 70: 31-48.

( Received 08 January 2016; accepted 29 January 2016 )

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7. SPECIES INDEX

Agelenidae Agelena barunae 13

Araneidae Arachnura angora 13 Araneus mitificus 14 Araneus nympha 14 Argiope aemula 15 Argiope pulchella 15 Chorizopes bengalensis 16 Cyclosa bifida 16 Cyclosa bilibata 17 Cyclosa insulana 17 Cyclosa mulmeinensis 18 Cyclosa neilensis 18 Cyclosa quinqueguttata 19 Cyclosa simony 19 Cyclosa spirifera 20 Cyclosa krusa 20 Cyrtarachne raniceps 21 Cyrtophora moluccensis 21 Cyrtophora exanthematica 22 Eriovixia excels 22 Gasteracantha diadesmia 23 Gasteracantha kuhlii 23 Gasteracantha unguifera 24 Gea zagarosa 24 Larinia chloris 25 Neoscona bengalensis 25 Neoscona mukerjei 26 Neoscona nautical 26 Neoscona theisi 27 Neoscona vigilans 27 Neoscona yptinica 28 Parawixia dehaani 28

Clubionidae Clubiona drassodes 29 Clubiona rama 29

Ctenidae Ctenus sikkimensis 30

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Eutichuridae Cheiracanthium himalayense 30 Cheiracanthium trivial 31

Gnaphosidae Zelotes pseudopusillus 31

Hersiliidae Hersilia savignyi 32

Linyphiidae Lepthyphantes rudrai 32

Lycosidae agelenoides 33 Hippasa greenalliae 33 Hippasa himalayensis 34 Lycosa phipsoni 34 Pardosa heteropthalma 35 Pardosa songosa 35

Nephilidae Herennia multipuncta 36 Nephila clavata 36 Nephila pilipes 37

Oxyopidae Oxyopes kamalae 37 Oxyopes naliniae 38 Oxyopes shweta 38 Oxyopes sitae 39

Pisauridae Dendrolycosa robusta 39 Dendralycosa gitae 40

Salticidae Carrhotus viduus 40 Epocilla aurantiaca 41 Hyllus semicupreus 41 Menemerus brevibulbis 42 Myrmarachne bengalensis 42 Myrmarachne caliraya 43 Phintella vittata 43 Plexippus paykullii 44 Plexippus pseudopaykullii 44

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Portia fimbriata 45 Rhene danieli 45 Rhene indica 46 Rhene rubrigera 46 Siler semiglaucus 47 Telamonia dimidiate 47 Thiana bhamoensis 48

Sparassidae Bhutaniella sikkimensis 48 Heteropoda andamanensis 49 Olios abesulus 49

Tetragnathidae Leucauge decorate 50 Leucauge tessellate 50 Opadometa fastigata 51 Tetragnatha caudicula 51

Theridiidae Chrysso urbasae 52 Theridion indicum 52

Thomisidae Camaricus formosus 53 Ozyptila khasi 53 Thomisus andamanensis 54

Uloboridae Miagrammopes nr. kirkeensis 54 Uloborus khasiensis 55

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BIOGRAPHY

DINENDRA RAYCHAUDHURI, is now serving the Department of Agricultural Biotechnology, IRDM Faculty Centre, Ramakrishna Mission Vivekananda University in the capacity of Honorary Professor following his retirement as Professor of Zoology, University of Calcutta, Kolkata. Raychaudhuri is one of the well known Entomologists having 205 articles on insects and spiders to his credit. Other than being author of several books, monographs and chapters, he has acted as mentor of 25 Ph.D. students. He is the recipient of several distinction and honours.

E-mail address: [email protected]

SUMANA SAHA, Associate Professor, Post Graduate Department of Zoology, Darjeeling Govt. College is equally a well known personality in the field Zoology, precisely Entomology. Her contributions is well acknowledged in the ambit of both academics and research. A dedicated researcher of the contemporary period, Saha is the author of 129 articles including books/monographs and popular articles. She has received few honours in these 25 years of research career.

E-mail address: [email protected]

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