earthworm communities of kashmir valley, india

Tropical Ecology 52(2): 151-162, 2011 ISSN 0564-3295 © International Society for Tropical Ecology www.tropecol.com

Earthworm communities of Kashmir Valley, India

ISHTIYAQ AHMED NAJAR & ANISA B. KHAN*

Department of Ecology and Environmental Sciences, Pondicherry Central University, Puducherry 605014, India

Abstract: Information available on the earthworm communities of Kashmir Valley, India, being limited, the present study evaluates the diversity, distribution and seasonal population density of earthworms in the Kashmir Valley, as well as interhabitat community variation. A total of eight earthworm species belonging to three different families. Moniligastridae, Megascolecidae and Lumbricidae were recorded. Out of eight species, three species: Aporrectodea caliginosa caliginosa, Octolasion cyaneum and Eisenia fetida are reported for the first time from Kashmir Valley. Earthworm population density varied significantly among the sites (F19,60 = 9.46, P < 0.05), among the seasons (F 3,76 = 3.64, P < 0.05) and ranged from 11 to 159 No. m-2. Earthworm population biomass also varied significantly among the sites (F19,60 = 11.01, P < 0.05), among the seasons (F3,76 = 3.2, P < 0.05) and ranged from 3.41 to 48.14 g m-2. Margalef species richness was 0.13 to 0.32, Shannon-Wiener diversity indices were 0.45 to 1.09 and Pielou's evenness 0.64 to 0.99. The number of species of earthworms was positively correlated with soil organic carbon (r = 0.539; P < 0.05), organic nitrogen (r = 0.724; P < 0.01) and moisture (r = 0.585; P < 0.01). These data suggest that the number of earthworm species is greater in those sites where organic carbon, organic nitrogen and moisture are higher, thus human-controlled systems exhibited higher diversity.

Resumen: La información disponible sobre las comunidades de lombrices de tierra del

Valle de Cachemira es limitada. El presente estudio evalúa la diversidad, la distribución y la densidad poblacional estacional de lombrices de tierra en el Valle de Cachemira, así como la variación de la comunidad entre hábitats. Se registraron en total ocho especies de lombriz de tierra pertenecientes a tres familias diferentes: Moniligastridae, Megascolecidae y Lumbricidae. Tres de las ocho especies (Aporrectodea caliginosa caliginosa, Octolasion cyaneum y Eisenia fetida) se reportan por primera vez para el Valle de Cachemira. La densidad poblacional de las lombrices de tierra varió significativamente entre sitios (F19,60 = 9.46, P < 0.05) y entre estaciones (F 3,76 = 3.64, P < 0.05), y fluctuó de 11 a 159 ind. m-2. La biomasa poblacional de las lombrices de tierra también varió significativamente entre sitios (F19,60 = 11.01, P < 0.05) y estaciones (F3,76 = 3.2, P < 0.05), y fluctuó de 3.41 a 48.14 g m-2. La riqueza de especies de Margalef varió entre 0.13 a 0.32, los índices de diversidad de Shannon-Weiner estuvieron entre 0.45 y 1.09, y la equitatividad de Pielou fluctuó de 0.64 a 0.99. El número de especies de lombrices de tierra se correlacionó positivamente con el carbono orgánico (r = 0.539; P < 0.05), el nitrógeno orgánico (r = 0.724; P < 0.01) y la humedad (r = 0.585; P < 0.01) del suelo. Estos datos sugieren que el número de especies de lombrices de tierra es mayor en sitios con mejor disponibilidad de carbono orgánico, nitrógeno orgánico y humedad, y por lo tanto los sistemas con control humano exhibieron una mayor diversidad.

Resumo: A informação disponível sobre as comunidades de minhocas no Vale de Caxemira,

Índia, é limitada, pelo que o estudo presente avalia a diversidade, distribuição e densidade sazonal da população de minhocas no vale de Caxemira, bem como a variação inter-habitats da comunidade. Registou-se um total de oito espécies de minhocas pertencentes a três famílias

N

* Corresponding Author; e-mail: [email protected]

152 EARTHWORMS OF KASHMIR VALLEY

distintas - Moniligastridae, Megascolecidae e Lumbricidae. Das oito espécies, três delas - Aporrectodea caliginosa caliginosa, Octolasion cyaneum e Eisenia fetida - foram registadas pela primeira vez no vale de Caxemira. A densidade da população de minhocas variou significa-tivamente entre os sítios (F19,60 = 9.46, P < 0.05), entres estações (F 3,76 = 3.64, P < 0.05) e o seu número variou entre as 11 e 159 m-2. A biomassa da população de minhocas também variou significativamente entre sítios (F19,60 = 11.01, P < 0.05), entre estações (F3,76 = 3.2, P < 0.05) e variou entre os 3,41 e os 48,14 g m-2. A riqueza específica de Margalef foi de 0,13 a 0,32, sendo os índices de diversidade de Shannon-Wiener de 0,45 a 1,09 com um índice de semelhança de Pielou de 0, 64 a 0,99. O número de espécies de minhocas estava positivamente correlacionado com o carbono orgânico do solo (r = 0.539; P < 0.05), com o azoto orgânico (r = 0.724; P < 0.01) e com a humidade (r = 0.585; P < 0.01). Estes dados sugerem que o número de espécies de minhocas é maior naqueles sítios com carbono orgânico, azoto orgânico e humidade mais alta e assim, os sistemas com controlo humano exibem uma diversidade mais elevada.

Key words: Biomass, diversity, earthworms, Kashmir Valley, population density.

Introduction

Earthworms are among the most important components of soil biota in terms of soil formation, maintenance of soil structure and fertility (Bhadauria & Saxena 2010). Although not numeri-cally dominant, their size makes them one of the major contributors to invertebrate biomass in soils (Edwards 2004). Approximately 4,400 different species of earthworms have been identified world-wide (Sinha 2009), with reports on diversity of earthworms in various parts of the world including those of Tsai et al. (2000); Blakemore (2003); Chang & Chen (2005); Blakemore et al. (2006); Sautter et al. (2006). Julka et al. (2009) reported 590 species of earthworms from India and al-though earthworms are well studied in other parts of India (Chaudhuri et al. 2008; Karmegam & Daniel 2007; Sathianarayanan & Khan 2006; Tripathi & Bhardwaj 2004; Bisht et al. 2003), there is paucity of information on the earthworms of Kashmir Valley, India. With limited reports on the earthworms of Kashmir Valley (Stephenson 1922; Sharma & Kaul 1974 and Paliwal & Julka 2005), the present study investigates the diversity and distribution of earthworms in Kashmir Valley. Besides studying the interhabitat variation of earthworm communities, this study also examines the seasonal variation in population density and biomass of earthworms across different sampling sites.

Materials and methods

Study area Kashmir Valley of the State of Jammu and

Kashmir, India (Fig. 1) is situated between 33° 15′ and 34° 30′ N latitude and 74° and 75° 13′ E longitude. It is a broad, open valley bounded on south by the Pir Panjal range and on the north by the main or central Himalayan ranges. Kashmir Valley lies in the temperate zone, characterized by wet and cold winter and relatively dry and moderate hot summer. The hottest months are July and August, when the maximum temperature rises above 30 °C. September has cooler nights and the severe winter sets in about the middle of December. The coldest month is January, with temperature falling below freezing point. The winters vary from year to year; some are severe with very heavy snowfall, while others are mild with moderate snowfall.

The study was conducted in 5 parts of Kashmir Valley viz. South Kashmir (Anantnag and Kul-gam), North Kashmir (Baramulla, Kupwara and Bandipore), South-east Kashmir (Pulwama and Shopain), North-west Kashmir (Budgam) and Central Kashmir (Srinagar and Ganderbal). This arrangement of districts is based on their geographical location, since there were no scientific reports on earthworm from these areas to base our sampling on. The year is divided into four

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seasons (Enex 1978) viz., winter (December-February), spring (March-May), summer (June-August) and autumn (September-November).

Fig. 1. Outline map of Kashmir Valley.

Study sites Earthworms were collected from 20 sites

(Table 1) each characterized by different vege-tation types, slopes and elevation between 1490 to 2450 masl. The sites included 5 vegetable gardens, 4 paddy (rice) cultivation, 2 Pinus forests, 2 Populus plantation, each 1 of maize cultivation, cattle pasture, flower gardens, saffron cultivation (Crocus sativus), apple orchard (Malus domestica), willow plantation (Salix alba) and chinar trees (Platanus orientalis). Study sites are well drained, with silt to sandy loamy soil texture (Hoon 1939).

Sampling for earthworms and soil was done every month at each site between 2007 and 2008. A sampling grid (50 m × 50 m) was established at each site, containing 25 units of 10 m × 10 m, which were further divided into subunits of 1 m2. These 1 m2 subunits were selected randomly at a distance of 8 m from each other and no subunit was sampled twice. Earthworms were collected by digging soil monolith (25 x 25 x 30 cm) and handsorting. Worms were sorted into clitellates, non-clitellates (> 4 cm, without clitellum but have genital markings) and juveniles (< 4 cm, lack of genital marking, tumescences and clitellum) (Zorn et al. 2005), counted, weighed, preserved in 4 % formalin and sent to Zoological Survey of India (ZSI) for identification.

Soil and data analysis Composite soil samples comprising of five sub-

samples were analyzed using following methods- soil temperature by soil thermometer and soil moisture by gravimetric method (Gupta 1999); pH, EC, calcium, magnesium by Versenate method and organic nitrogen by micro Kjeldahl method (Jackson 1973); soil texture by the international pipette method (Gee & Bauder 1986); organic carbon (Walkley & Black 1934), total sodium and potassium by flame photometry (Simard 1993) and phosphorous by Anderson & Ingram (1993).

The Margalef species richness DMg (D=S-1/ln N, where, S is number of species and N is number of individuals), Shannon and Wiener diversity index H′ (H′= -Σpi ln pi, where, pi the proportional abundance of the ith species = ni/N) and Pielou's evenness E (E= H′/ ln S, where, H′ is Shannon and Weiner diversity index and S is number of species) were calculated for each site (Magurran 2004). Variation in population density and biomass of earthworms across sampling sites and among seasons was tested using one-way ANOVA. Pearson correlation coefficient (r) was employed to examine the relationship between number of earthworm species, population density and biomass with soil physico-chemical parameters.

Results The results of the present study reveals a total

of 8 species of earthworms belonging to 5 genera, three families and two orders under class Oligochaeta. Among these, 6 species belong to family Lumbricidae (Aporrectodea caliginosa cali-ginosa, Aporrectodea caliginosa trapezoides, Apor-rectodea parva, Aporrectodea rosea rosea, Eisenia fetida, and Octolasion cyaneum), one species belongs to the family Megascolecidae (Amynthus cortices) and one species belongs to the family Moniligastridae (Drawida japonica).

Ecological category, food, size and morpho-logical characteristics of earthworm species of Kashmir Valley are given in Table 2. Among the earthworm species recorded, A. parva and E. fetida are epigeic whereas A. corticis, D. japonica, A. c. caliginosa, A. c. trapezoides, A. r. rosea and O. cyaneum are endogeic (Stephensen 1923).

The distribution of earthworm species in Kash-mir Valley with respect to soil ecological para-meters - temperature, moisture, pH, soil organic carbon, total organic nitrogen, total phosphorous,

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Table 5. Species richness, Diversity index, Evenness and No. of species of earthworms at different study sites.

Site Number of species

Species richness ( DMg)

Diversity index (H´)

Evenness (E´)

South Kashmir Pinus forest

2

0.13

0.63

0.91

Paddy cultivation 2 0.13 0.45 0.64 Populus plantation 2 0.14 0.56 0.81 Vegetable garden 2 0.15 0.63 0.91

North Kashmir Pinus forest 2 0.14 0.46 0.66 Maize cultivation 2 0.15 0.60 0.87 Pasture 2 0.13 0.48 0.69 Vegetable garden 2 0.15 0.54 0.77

North-west Kashmir Flower garden

3

0.30

1.09

0.99

Paddy cultivation 2 0.15 0.59 0.84 Vegetable garden 3 0.28 0.86 0.78 Willow plantation 2 0.16 0.57 0.83

South-east Kashmir Apple orchard

0

-

-

-

Paddy cultivation 2 0.15 0.66 0.95 Saffron cultivation 0 - - - Vegetable garden 2 0.14 0.60 0.86

Central Kashmir Chinar trees

2

0.15

0.66

0.96

Paddy cultivation 2 0.14 0.62 0.89 Populus plantation 3 0.32 1.04 0.95 Vegetable garden 2 0.14 0.56 0.81

total sodium and potassium is given in Table 3. Earthworms were present within the range of soil temperature 8 - 12.38 °C, moisture 15.50 - 33.88 %, pH 5.9 - 8.23, EC 0.09 - 0.38 mS cm-1, Ca 2.52 - 4.68 g kg-1, Mg 0.38 - 1.24 g kg-1, Na 9.84 - 41.15 µg g-1, K 3.46 - 24.34 µg g-1, TP 314.89 - 700.55 µg g-1, OC 18 - 30.7 g kg-1, and ON 0.6 - 2 g kg-1.

In terms of distribution, A. r. rosea was present at 14 sites, A. c. trapezoides at 13 sites, D. japonica at 4 sites, E. fetida at 3 sites, A. corticis at 2 sites, O. cyaneum, A. c. trapezoides and A. parva each at one site. Earthworms were absent at site no. 13 and 15 (Table 4).

Margalef species richness ranged from 0.13 at paddy cultivation site (South Kashmir) to 0.32 at Populus plantation site (Central Kashmir). The Shannon-Weiner diversity index ranged from 0.45 at paddy cultivation site (South Kashmir) to 1.09 at flower garden site (North-west Kashmir), where as Pielou's evenness ranged from 0.64 at paddy cultivation site (South Kashmir) to 0.99 at flower

garden site (North-west Kashmir): (Table 5). Population density and biomass of earthworms

at different sites during different seasons is depicted in Fig. 2 and Fig. 3. Population density varies significantly among the sites (F19,60 = 9.46, P < 0.05) and among the seasons (F3,76 = 3.64, P < 0.05). Biomass also varies significantly among the sites (F19,60 = 11.01, P < 0.05) and among the seasons (F3,76 = 3.2, P < 0.05). Population density ranges from 11 No. m-2 at maize cultivation site (North Kashmir) during summer with biomass range of 3.41 g m-2 to 159 No. m-2 with biomass 48.14 g m-2 at cattle pasture site (North Kashmir) during spring.

Discussion Out of 8 species of earthworms reported,

three (O. cyaneum, E. fetida, and A. c. caliginosa) are new reports to the checklist of earthworms of Kashmir Valley. The earthworm species D. japo-nica, O. cyaneum, A. parva, A. c. trapezoides, A. r.

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1=Pinus forest, 2=Paddy cultivation, 3=Populus plan-tation, 4=Vegetable garden (South Kashmir); 5= Pinus forest, 6= Maize cultivation, 7=Pasture, 8=Vegetable garden (North Kashmir); 9=Flower garden, 10=Paddy cultivation, 11=Vegetable garden, 12=Willow plantation (North-west Kashmir); 13=Apple orchard, 14=Paddy cultivation, 15=Saffron cultivation, 16=Vegetable garden (South-east Kashmir); 17=Chinar trees, 18=Paddy cultivation, 19=Populus plantation, 20=Vegetable garden (Central Kashmir). Fig. 2. Population density (No. m-2) of earthworms at different sites during different seasons. rosea, E. fetida, and A. corticis are also reported from other parts of Western Himalayas viz., Himachal Pradesh and Uttaranchal, while A. c. caliginosa is reported from Himachal Pradesh (Paliwal & Julka 2005).

Out of 8 species, A. r. rosea and A. c. trapezoides are present at the maximum number of sites and exhibit a wide range of tolerance to edaphic factors. Tischer (2008) reported A. r. rosea most widespread and abundant earthworm in agricultural soils. A. c. trapezoides is predominant in areas disturbed by human activities (Misirugolu 2004; Sims & Gerard 1999). In the present study A. c. trapezoides was present primarily in human-controlled ecosystems. However, O. cyaneum, A. c. caliginosa, A. parva were restricted to only one site each. Sims & Gerard (1999) report that O. cyaneum prefers moist habitats in Great Britain. In the present study O. cyaneum is restricted to chinar trees site (Central Kashmir) and it is one of

1=Pinus forest, 2=Paddy cultivation, 3=Populus plan-tation, 4=Vegetable garden (South Kashmir); 5= Pinus forest, 6= Maize cultivation, 7=Pasture, 8=Vegetable garden (North Kashmir); 9=Flower garden, 10=Paddy cultivation, 11=Vegetable garden, 12=Willow plantation (North-west Kashmir); 13=Apple orchard, 14=Paddy cultivation, 15=Saffron cultivation, 16=Vegetable garden (South-east Kash-mir); 17=Chinar trees, 18=Paddy cultivation, 19=Populus plantation, 20=Vegetable garden (Cen-tral Kashmir). Fig. 3. Biomass (g m-2) of earthworms at different sites during different seasons. the sites (Table 3) having higher levels of moisture indicating that O. cyaneum prefers the habitat with higher levels of moisture and relatively cooler temperatures. The presence of species in a particular habitat and its absence from other habitats shows the species-specific distribution of earthworms in different pedoecosystems. Similar observation was reported in the species composition of earthworms in different grasslands, cultivated and forest soils (Singh 1997). Mathieu et al. (2010) also reported that earthworms prefer habitats of high quality (in terms of environmental conditions) and that habitat quality actually affects earthworm fitness (Lowe & Butt 2005). Earthworms were absent in apple orchard and saffron cultivation sites (South-east Kashmir). The low nitrogen content of soil in the apple orchard may be responsible, as nitrogen is often considered a critical factor limiting earthworm populations in many temperate ecosystems (Curry 2004). The low


moisture content of soil at saffron cultivation site might be a reason for their absence in this ecosystem. This is consistent with the report of Smetak et al. (2007) that relatively low soil moisture is of concern as earthworms are parti-cularly sensitive to moisture stress and relay on soil water to stay hydrated. Soil moisture, pH, organic carbon and organic nitrogen play impor-tant role in the distribution of earthworms (Decaens et al. 2003). Soil pH in this study varied from moderate acidic to moderate alkaline (5.9 to 8.2), (Table 5). Chaudhuri & Bhattacharjee (1999) reported earthworms are mostly distributed in a pH range of slightly acid to moderate alkaline, thus pH value recorded in the present study are within the range for the distribution of earth-worms.

Earthworm diversity tended to be low with one to three species present within the sites. Low earthworm species diversity with the site is not uncommon. Most earthworm diversity studies report the presence of between two to five species at any one location (Edwards & Bohlen 1996; Fragoso & Lavelle 1992; Lee 1985). The occurrence of maximum number of species at flower garden site (North-west Kashmir), vegetable garden site (North-west Kashmir) and Populus plantation site (Central Kashmir) as compared to other pedo-ecosystems is supported by higher moisture, organic carbon and nitrogen. Significant corre-lations were obtained between the number of earthworm species and organic nitrogen (r =0.724; P < 0.01), with moisture (r = 0.585; P < 0.01) and with organic carbon (r = 0.539; P < 0.05). This is consistent with previous research that established correlations between diversity and organic carbon (Edwards & Bohlen 1996; Hendrix et al. 1992; Sinha et al. 2003).

Margalef species richness, Shannon-Weiner diversity index and Pielou's evenness are higher at flower garden site (North-west Kashmir), vege-table garden sites at North-west Kashmir and Central Kashmir, this may be related to higher moisture, carbon and nitrogen content of soil. Similarly Tripathi & Bhardwaj (2004) have reported higher diversity indices and evenness in cultivated soils.

Population density and biomass of earthworms vary significantly among the sites and among the seasons. This indicates that sites and as well as seasonal difference, may influence earthworms in a significant way. Population density ranges from 11 No. m-2 at maize cultivation sites during summer with biomass 3.41 g m-2 to 159 No. m-2

with biomass 48.14 g m-2 at pasture sites (North Kashmir) during spring. This may be related to the optimum moisture and temperature conditions that prevailed. This is supported by the work of Callaham & Hendrix (1997) as they reported earthworms were most abundant during spring. Population density was minimum during winter at Pinus forest site, paddy cultivation site, Populus plantation site (South Kashmir); Pinus forest site, cattle pasture site (North Kashmir); willow plantation site (North-west Kashmir); vegetable garden site (South-east Kashmir) and chinar trees, paddy cultivation, Populus plantation sites (Central Kashmir), which is attributed to low temperature during winter as delay in hatching of cocoons at low temperature and Timmerman et al. (2006) also reported low earthworm abundance during winter due to the low temperature. Population density was also minimum during summer at maize plantation (North Kashmir), flower garden (North-west Kashmir), paddy cultivation (North-west Kashmir and South-east Kashmir). One of the reasons might be low mois-ture content of soil during that season as fecundity of earthworms is greatly influenced by low soil moisture. Schmidt & Curry (2001) reported low population levels with low moisture content of soil. The low population density at vegetable gardens (South and North Kashmir) during autumn and at vegetable garden (Central Kashmir) during sum-mer could be attributed to the mechanical damage due to ploughing. Pfiffner & Luka (2007) reported decrease in number of earthworms after plou-ghing, as it causes mechanical damage and mechanical disturbance that can lead to unstable microclimatic conditions and abrasive effects in the soil profile, as well as the removal of protective surface residues.

Conclusions Of the eight species reported in the study, only

two were epigeic species (E. fetida and A. parva) and six were endogeic (A. corticis, D. japonica, A. c. caliginosa, A. c. trapezoides, A. r. rosea and O. cyaneum). A. r. rosea and A. c. trapezoides exhi-bited a wide distribution range whereas O. cya-neum, A. c. caliginosa, A. parva showed restricted distribution. Vegetable gardens harbor maximum number of earthworm species whereas earthworms were absent at apple orchard and saffron cultivation sites. This may be due to the influence of edaphic factors like organic carbon, organic nitrogen and moisture that play a significant

NAJAR & KHAN 161

role in distribution of earthworms. Thus human-controlled systems exhibited higher diversity and extremely low temperature appears to be limiting factor during winter. Number and biomass of earthworms vary significantly among the sites and among the seasons, thus climate and soil physicochemical characteristics play a signi-ficant role in earthworm communities of Kashmir Va-lley.

Acknowledgements Authors express thanks to Dr. J. M. Julka and

Dr. R. Paliwal of Zoological Survey of India, for taxonomic identification of the earthworm species and Dr Abdul Hai, Head, Hydrobiology Research Laboratory, Kashmir, for providing laboratory faci-lities.

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earthworm communities of kashmir valley, india

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