ASIAN J. EXP. BIOL. SCI.

VOl 1 (2) 2010: 360 - 369

Society of Applied Sciences

ORIGINAL ARTICLE

Human-induced Biological Invasions in Rubber (Hevea brasiliensis) Plantations of Tripura (India) - Pontoscolex corethrurus as a Case study
Sabyasachi Nath & P.S. Chaudhuri* Department of Zoology, Maharaja Bir Bikram College, Agartala 799004, Tripura, India. Email: priya_1956@rediffmail.com
ABSTRACT The study on earthworm invasion in the tropics due to anthropogenic land use change is limited. Afforestation of wasteland or fallows through rubber (Hevea brasiliensis) plantation in Tripura (India) played a major role in determining the abundance and community characteristics of earthworms and the establishment of the exotic earthworm, Pontoscolex corethrurus in areas previously inhabited by endemic earthworms. Factors contributing to invasion of P. corethrurus in rubber plantations may include anthropogenic disturbances (viz. forest clearance, taping etc.), individual tree species effect, competitive interaction between the exotic and the endemic species and their reproductive strategies. With increase in the age of rubber plantation, densities and biomasses of P. corethrurus increased and those of endemic earthworm community decreased significantly (p<0.01). Relative abundance of P. corethrurus also increased significantly with the increasing age of rubber plantations making it a eudominant species of rubber plantation according to Engelmanns scale of dominance. Exotic species invasion in rubber plantation also led to increase in the index of dominance and decrease in Shannon diversity index and species evenness with increase in the age of rubber plantation. Keywords: Invasive species, Pontoscolex corethrurus, rubber plantation, density, biomass, index of dominance, Shannon-diversity index.

INTRODUCTION Biological invasions have recently become a major research issue in ecology, particularly due to deleterious or unknown effect that exotic species may have on the health and functioning of ecosystem. Invasive species successful at establishment, spread typically with lack of checks on population growth and can have important ecological consequences in the long run [1]. Land use history always plays a major role in determining the abundance and community structure of earthworms and the establishment of exotic earthworms in areas previously inhabited by endemic earthworms. For example, in the tropics, conversion of forest to pasture has been associated with significant decrease in soil macro-invertebrate diversity [2] and with the dominance of a few exotic earthworm species following disturbance [3]. Many native species are in danger of extinction or have already disappeared in Amazonia due to the colonization by exotic species of earthworms [4]. Rubber plant (Hevea brasiliensis) was brought to Tripura in 1963 to check soil degradation due to slash and burn agriculture practiced by the local tribal people and also as a part of their rehabilitation programme. According to a recent report, Pontoscolex corethrurus was the most dominant species and represented 61.5% biomass and 72% density of the total earthworm community in rubber plantations of Tripura [5]. P. corethrurus (Glossoscolecidae), indigenous to north-eastern South America, is now a dominant invasive species around the world where exotic crops or new agricultural techniques have been introduced [1]. In Puerto Rico, P. corethrurus invaded primary cloud forests at the top of the Luquillo Mountains [6]. All the disturbed agro-ecosystems of Mexico, Costa Rica, Peru, Brazil, Congo etc. are dominated by P. corethrurus and there are some instances of total replacement of native species as well [7]. The invasions of exotic earthworms in the tropics can be explained to a

360

Human-induced Biological Invasions in Rubber Plantations of Tripura

Nath & Chaudhuri

great extent by the historical dispersal of humans and commerce (e.g., trade routes). Reforestation programs using root-ball planting stock provide another means of dispersal of exotic species [8]. The aim of our present investigation is to understand the impact of human induced exotic earthworm invasion on the endemic earthworm communities in the rubber plantations of different age groups, using Pontoscolex corethrurus as a case study. MATERIALS AND METHODS Study area Survey was conducted during 20072008 (JuneNovember) in three subdivisions (Belonia, Khowai and Bishalgarh) in the West district of the state of Tripura, in North-east India (22512432N and 90109221E). Tripura having an area of 10,491 sq. km. experiences a subtropical climate with a mean annual temperature of 25C and average annual rainfall of 2000 mm. Study sites Study sites selected for earthworm survey comprised rubber plantations of three age groups viz. 10 year-old, 22 year-old and 35 year-old plantations located in Belonia, Khowai and Bishalgarh subdivisions. Only one rubber plantation was selected in each subdivision. Replications were not kept due to non-availability of same age group of plantation with more or less similar characteristics in the subdivisions. Historically each of the three age groups of rubber plantations was derived from afforestation of waste lands. The 10 year-old (2 ha area) and 35 year-old (2 ha) rubber plantations comprised undulating landscapes with small uplands locally called tilla while 22 year-old plantation (1 ha) was low plain land. The rubber trees were spaced in rows at a distance of 4.55.0 m from each other. The rubber plantations possess good canopy cover and horizontal distribution of roots in the topsoil. The plantation floor remained covered with Hevea leaf litter during most part of the year. Flow of rubber latex starts at 7 years age of plantation, becomes maximum at 20 years and typically ceases at 35 years of age of plantation. Rubber plantations often face anthropogenic interferences such as intermittent weeding, collection of leaf litter for using as fuel by local tribal people, latex harvesting etc. Although H. brasiliensis was the dominant species of the rubber plantation, a few other plant species including herbs and shrubs viz. Chromolaena odorata (L.), Hyptis suaveolens Pilot, Lantana camera L., Lygodium flexuosum (L.) Sw, Mimosa pudica L. etc. were also found. The soils of rubber plantations were strongly acidic indicating that these have developed from non-calcareous parent material under conditions of high rainfall [9]. Sampling of earthworm population Sampling was done every alternate Saturday of a month during monsoon (JuneSeptember) and post monsoon period (20072008). For each study site, a total of forty samples were taken randomly. Initially diluted formalin was applied [10], but it was found to be less effective to extract earthworms from the soils of rubber plantations, thus indicating the absence of the anecic earthworms (vertical burrower) in rubber plantations in Tripura. Later, earthworms were collected by conventional digging (252530cm) and hand sorting method (only method considered in our present study). They were counted, weighed (with gut content) in an electronic balance and some were preserved in 5% formalin. For conservation of biodiversity, minimum numbers of worms (1015) were preserved from each study site and others were released back to the soil. Results were expressed in terms of biomass (fresh weight g. m-2) and density (individual m-2). Relative abundance, species richness index, index of dominance and diversity index of earthworms in the different age groups of rubber plantations were determined [11]. Dominance of species was evaluated on the basis of relative abundance using Engelmanns scale [12]. Soil analysis Soils were collected by scraping the walls of the quadrat pits from 015 cm depth with a metal shovel and were subjected to analysis of different physico-chemical properties e.g., soil moisture (gravimetric wet weight method), pH (1: 2.5 dilution method) and soil organic matter [13]. Soil temperatures were recorded in situ at each sample plot at a depth of 15 cm. Soil texture was determined by Bouyoucos hydrometer. Data analysis

361

Human-induced Biological Invasions in Rubber Plantations of Tripura

Nath & Chaudhuri

Variations in densities and biomasses of P. corethrurus and endemic earthworms among different age groups of rubber plantations were tested by Students t-test. The relationship between population size (density and biomass) of earthworms and age of rubber plantations was expressed by bar diagrams. The correlations between soil parameters and population size of earthworms were calculated as a simple correlation coefficient (r). RESULTS Site characteristics Both the ten year-old and thirty five year-old rubber plantations had sandy loam soil (sand 80%, clay 13%, silt 7%), while twenty two year-old rubber plantation showed sandy soil (sand 88%, clay 3%, silt 9%) texture. Temperature, moisture, pH and organic matter did not differ significantly (p>0.05) among different age groups of plantations (Table 1). Community structure From the three study sites a total of eleven species were identified. These belonged to five families [Moniligastridae three species (Drawida assamensis, D. papillifer papillifer, Drawida sp), Megascolecidae two species (Metaphire houlleti, Kanchuria sp), Octochaetidae four species (Eutyphoeus comillahnus, E. gigas, E. scutarius, Octochaetona beatrix), Glossoscolecidae one species (Pontoscolex corethrurus) and Ocnerodrilidae one species (Gordiodrilus elegans)]. Kanchuria sp is a new species and will be described soon. Only four species i.e., P. corethrurus, M. houlleti, Kanchuria sp and E. comillahnus were common to all the three plantations of different age groups. Of the eleven species recorded, P. corethrurus and G. elegans are exotic, whereas the rest nine species are endemic to the Indian subcontinent. P. corethrurus was the dominant species in each of the three age groups of rubber plantations. In spite of deciduous litter fall, most of the earthworm species of rubber plantations were endogeic (geophagous) and only M. houlleti was epianecic (phytogeophagous). No epigeic or anecic earthworm species were recorded from the soils of rubber plantations. Interhabitat variation in community characteristics Number of earthworm species found in different habitats were nine in 10 year-old plantation (viz. P. corethrurus, Kanchuria sp, M. houlleti, E. comillahnus, E. scutarius, D. assamensis, D. papillifer papillifer, Drawida sp and G. elegans), five in 22 year-old plantation (viz. P. corethrurus, Kanchuria sp, M. houlleti, E. comillahnus, D. assamensis) and seven in 35 year-old plantation (viz. P. corethrurus, Kanchuria sp, M. houlleti, E. comillahnus, E. gigas, O. beatrix, D. p. papillifer). Species richness index after sudden decline from 0.75 in 10 year-old rubber plantation to 0.36 in 22 year-old plantation, marginally increased to 0.43 in 35 year-old plantation. Biomass, densities and relative abundance of earthworm populations under the different age groups of plantations are given in the Table 2. Although there were no significant differences (p>0.05) in the total earthworm biomasses among the three age groups of plantations, total earthworm densities increased significantly (p<0.05) with increase in the age of rubber plantation (Table 1). In our present study, in the 10 year-old plantation total densities and total biomasses of endemic species (7 species together) were much higher than those of exotic P. corethrurus. Later total densities and biomasses of endemic species decreased and those of P. corethrurus increased significantly (p<0.01) with increase in the age of rubber plantations (Fig 1). Densities of P. corethrurus were 37.7616.14, 94.085.78 and 161.2818.40 in the 10 year-old, 22 year-old and 35 year-old plantations which comprised 41%, 78% and 96% of earthworm densities in the respective age groups of plantations. Total densities of endemic species were 54.409.12, 26.242.75 and 6.401.43 in the 10 year-old, 22 year-old and 35 year-old plantations respectively that comprised 59%, 22% and 4% of earthworm densities in the respective age groups of plantations. In the 10 year-old, 22 year-old and 35 year-old plantations, biomasses of P. corethrurus were 14.045.97, 34.182.39 and 56.494.96 respectively that represented 26%, 58% and 88% of total earthworm biomasses in the respective age group of rubber plantations. Biomasses of endemic species were 39.057.40, 24.133.16 and 7.661.28 representing 74%, 42% and 12% of total earthworm biomasses in the 10 year-old, 22 yearold and 35 year-old plantations respectively. Relative abundances of the endemic species were very low and declined with increase in the age of rubber plantations (Table 1). Relative abundance of the exotic species P. corethrurus increased significantly (p<0.01) from 34 in the 10 year-old plantation to
362

Human-induced Biological Invasions in Rubber Plantations of Tripura

Nath & Chaudhuri

78 and 96 in the 22 year-old and 35 year-old rubber plantations respectively. On the basis of relative abundance P. corethrurus was the eudominant species in each of the three age groups of rubber plantations according to Engelmanns scale of dominance.Index of dominance increased and Shannon diversity index decreased with the increase in the age of rubber plantations (Table 1). Interestingly, in the index of dominance, contribution of the exotic species, P. corethrurus was 74%, 95% and 100% in the 10 year-old, 22 year-old and 35 year-old rubber plantations respectively. Earthworms/soil properties relationship There was a significant positive correlation between soil temperature and population size (density and biomass) of P. corethrurus (Fig 2). Endemic earthworms in general had significant (p<0.01) negative correlation between soil temperature and density (r=0.50, p<0.01) as well as soil temperature and biomass (r=0.48, p<0.01). Soil pH showed significant negative correlation with population size of P. corethrurus (Fig 3) and positive correlation with that of endemic earthworms (pH vs density, r=0.59, p<0.01; pH vs biomass, r=0.65, p<0.01). Soil moisture and soil organic matter showed least correlation with population size of P. corethrurus. Table 1. Some biosynecological parameters of 3 rubber plantations of different age group. Parameters
Soil texture

10 year-old
Sandy clay loam

22 year-old
Sandy

35year-old
Soil clay loam

Soil temperature (C) Soil moisture (%) Soil pH Soil organic matter (%) Earthworms density (No. m-2) Earthworms biomass (live wt. g. m ) Index of Dominance (c) Shannon Diversity index (H ) Species richness index (d) Mean SE
-2

25.580.14 26.392.57 5.050.05 1.390.15 92.1613.63 53.093.49 0.23 1.58 0.75

25.840.07 22.830.85 4.950.02 1.360.12 120.327.48 58.302.03 0.64 0.70 0.36

26.940.04 21.751.15 4.230.03 1.310.06 167.6818.89 64.154.74 0.93 0.22 0.43

Table 2. Density, biomass and relative abundance of earthworm species of different age groups of rubber plantations.
Earthworm Species P. corethrurus Age group Density (ind. m-2) Biomass (g. m-2) 14.045.97 34.182.39 56.494.96 5.632.64 6.081.84 3.321.45 0.960.96 3.012.13 0.740.74 Relative abundance (%) 34.1014.19 78.241.55 96.120.86 2.661.32 2.230.58 1.720.81 0.530.53 1.470.95 0.540.54

10 yrs- 37.7616.14 22 yrs- 94.085.78 35 yrs- 161.2818.40 10 yrs- 2.561.20 22 yrs- 2.560.64 35 yrs- 2.561.20 10 yrs- 0.640.64 22 yrs- 1.921.28 35 yrs- 1.281.28

Kanchuria sp

M. houlleti

363

Human-induced Biological Invasions in Rubber Plantations of Tripura

Nath & Chaudhuri

D. assamensis

10 yrs- 15.362.35 22 yrs- 19.842.75 35 yrs10 yrs- 17.283.14 22 yrs35 yrs- 0.64 10 yrs- 10.242.12 22 yrs35 yrs10 yrs- 1.921.28 22 yrs- 1.920.78 35 yrs- 0.64 10 yrs22 yrs35 yrs- 0.64 10 yrs- 0.64 22 yrs35 yrs10 yrs22 yrs35 yrs- 0.64 10 yrs- 5.762.12 22 yrs35 yrs-

10.531.68 10.561.55 9.091.41 0.34 3.390.73 4.162.66 4.482.02 0.34 2.50 4.99 0.44 0.290.10 -

17.752.59 16.371.68 19.833.51 0.43 13.954.85 2.031.40 1.690.71 0.27 0.43 1.54 0.50 7.613.07 -

D. p. papillifer

Drawida sp

E. comillahnus

E. gigas

E. scutarius

O. beatrix

G. elegans

Mean SE

364

Human-induced Biological Invasions in Rubber Plantations of Tripura

Nath & Chaudhuri

Fig 1. Bar diagram showing variations in (a) density and (b) biomass values of P. corethrurus and endemic species in 3 different age groups of rubber plantation.

Fig 2(a)

Fig 2(b)

Fig 2. Linear regression analysis between (a) soil temperature and density and (b) soil temperature and biomass of P. corethrurus in rubber plantations.

365

Human-induced Biological Invasions in Rubber Plantations of Tripura

Nath & Chaudhuri

Fig 3(a)

Fig 3(b)

Fig 3. Linear regression analysis between (a) soil pH and density and (b) soil pH and biomass of P. corethrurus in rubber plantations.
DISCUSSION Since rubber plantations in the studied area were derived from afforestation of wastelands, original earthworm fauna were retained in rubber plantation at the initial stages of their establishment. According to a report, tree plantations may influence earthworm abundance by altering the chemical and/or physical properties of soil such as the temperature, moisture, pH, organic matter levels and litter inputs [14]. Among different soil properties, pH is particularly an important determinant of earthworm population density and biomass [15]. Our present study revealed significant negative correlation between soil pH and population size of exotic species P. corethrurus. Thus highly acidic soils (pH<5.0) of rubber plantations favoured the population density and biomass of P. corethrurus in place of endemic earthworms. A recent report revealed significantly higher densities of P. corethrurus compared to other species in highly acidic soil (pH<5.0) in Maricao state forest, Puerto Rico [16]. Significant positive correlation between soil temperature and population size of P. corethrurus is an indicative of its high temperature tolerance. How an exotic species like P. corethrurus appeared in the rubber plantations of Tripura, a northeastern state of India? It is well known that the place of origin of rubber plant, H. brasiliensis was Brazil. P. corethrurus inhabiting the litter and soils of the tropical rain forests of South America and presumably indigenous to north-eastern South America, now occurs sporadically throughout the tropics mainly where exotic crops or new agricultural techniques have been introduced [17]. There
366

Human-induced Biological Invasions in Rubber Plantations of Tripura

Nath & Chaudhuri

were reports on the occurrence of the exotic species, P. corethrurus in the rubber plantations of Malaysia, Burma and South India as well [18, 19]. It is possible that large scale introduction of Para Rubber in the late 19th century into South-east Asia might have accelerated the expansion of its range [20]. Occurrence of exotic species, P. corethrurus with high density and biomass values in each of the three age groups of rubber plantations might be due to anthropogenic practices such as forest cleaning, weeding and taping. In fact, there are many instances of exotic species invasions in disturbed sites [8]. However, it is difficult to say whether disturbance is a necessary prerequisite for exotic species invasion. Factors contributing to exotic species invasion in the rubber plantations may also include individual tree species effect [21] that fovoured the exotic species P. corethrurus over other species of earthworms, as well as competitive interaction between the exotic and the endemic species. The last factor is important because density and biomass of the exotic earthworm, P. corethrurus increased and those of native earthworm communities decreased significantly with increase in the age of rubber plantations. At eight sites in Caribbean coast of Costa Rica that had a large human immigration and agricultural expansion, an increase in the size of P. corethrurus population corresponded significantly with reduction in the rest of earthworm fauna [22]. Earthworm density contributed mainly by P. corethrurus in the 35 year-old rubber plantation of Tripura is comparable to earthworm densities in the forests in Western ghat [23], tropical rain forests in Mexico [24], 20 year-old rubber plantation in Cote d Ivore [25] and mixed forest in central Himalaya [26]. Sudden drop in species richness in the 22 year-old rubber plantation compared to the 10 year-old plantation is not clear and might be linked to smaller sampling area and age-related changes in the chemical constituents of plant materials. The soil of the studied rubber plantations (especially those of 10 year-old plantation) retained a number of endemic species viz. Kanchuria sp, D. assamensis, D. papillifer papillifer, Drawida sp, E. comillahnus, E. scutarius, M. houlleti due to the fact that these plantations in Tripura have developed through afforestation. Occurrence of Kanchuria sp, E. comillahnus and M. houlleti along with the exotic species, P. corethrurus in each of the three age groups of plantations indicated that these endemic species had the ability to coexist with the exotic species under rubber plantations in Tripura. Disturbed sites with a combination of both endemic and exotic species have also been documented by some authors [14, 22, 27]. Absence of epigeic and anecic species in the rubber plantations might be related to less palatable nature of rubber leaf litter which are rich in polyphenol contents [28, 29]. Trend to decrease in the diversity index of earthworms was related to the sharp increase in the index of dominance of earthworms mainly contributed by P. corethrurus with the increasing age of rubber plantations. In fact, opportunity for invasion in disturbed ecosystems occurs when endemic earthworms leave vacant niche spaces that are available for colonization of exotic species [30]. The reproductive biology of exotic species may be considered in the context of invasion. Tropical exotic peregrine earthworms (e.g., P. corethrurus, Dichogaster modiglianii etc.) are considered to be continuous breeders with high fecundity, short incubation period and high hatching success [31]. Thus on the basis of response to selection pressure, their characteristics are probably adaptive strategies of r-selected organisms that enable them to survive in drastic environmental changes especially heat, draught and predation in the soil [31, 32]. Exotic endogeic species (e.g., P. corethrurus, Polypheretima elongata) have also been shown to increase their rate of cocoon production and incubation period with increasing temperature [31]. Parthenogenesis is common to most of the tropical earthworms including P. corethrurus [7]. Another characteristic that make P. corethrurus a successful invader is its ability to enter diapause under draught conditions [8]. Besides environmental plasticity parthenogenetic mode of reproduction, capacity to tolerate anthropogenic practices, efficient assimilation of low-quality soil organic matter, continuous breeding with high fecundity, high hatching success etc. could be adaptive strategies of tropical exotic earthworm like P. corethrurus to cope with harsh environments making them undoubtedly strong invaders [33].

ACKNOWLEDGEMENTS The authors express their sincere thanks to Professor Madhab Ch. Dash, Vice Chancellor (Retd.), Sambalpur University for his valuable comments and suggestions on the manuscript. The authors also express their sincere thanks to Dr. R. Paliwal, Zoological Survey of India, Kolkata 700016 for identification of earthworm species. Financial assistance from the Department of Science and
367

Technology, New Delhi (scheme No. SR/SO/AS-25/2005 dt. 03.11.06) in the form of fellowship to the first author is gratefully acknowledged.

REFERENCES
[1] [2] [3] [4] [5] [6] [7] Hendrix, P.F. & Bohlen, P.J. (2002). Exotic earthworm invasions in North America: Ecological and Policy implications. Bioscience, 52: 801-811. Lavelle, P. & Pashanasi, B.M. (1989). Soil macrofauna and land management in Peruvian Amazonia. Pedobiologia, 33: 283-291. Sanchez-De Leon, Y., Zou, X., Borges, S. & Ruan, H. (2003). Recovery of native earthworms in abandoned tropical pastures. Conservation Biology, 17: 999-1006. Lavelle, P. & Lapied, E. (2003). Endangered earthworms of Amazonia: an homage to Gilberto Righi. Pedobiologia, 47: 417-419. Chaudhuri, P.S., Nath, S. & Paliwal, R. (2008). Earthworm population of rubber plantations (Hevea brasiliensis) in Tripura, India. Tropical Ecology, 49: 225-234. Hendrix, P.F., Lachnicht, S.L., Callaham, M.A.Jr. & Zou, X.M. (1999). Stable isotopic studies of earthworm feeding ecology in tropical ecosystems of Puerto Rico. Rapid Commun Mass Spectrometry, 13: 1295-1299. Fragoso, C., Lavelle, P., Blanchart, E., Senapati, B.K., Jimenez, J.J., Martinez, M.A., Decaens, T. & Tondoh., J. (1999). Earthworm Management in Tropical Agroecosystems (Eds. Lavelle, P., Brussaard, L. and Hendrix, P.), CAB International, Wallingford, UK., pp 27-55. James, S.W. & Hendrix, P.F. (2004). Earthworm Ecology (Ed. Edwards, C.A.), St. Lucie Press, Boca Raton, Florida pp. 75-87. Chaudhury, M., Sarma, A.C., Pal, T.K., Chakraborty, S.K. & Dey, S.K. (2004). Available nutrient status of the rubber growing soils in the lower Brahmaputra valley of Assam. Natural Rubber Research, 17(2): 177-179. Raw, F. (1959). Estimating earthworm population by using formalin. Nature, 21: 1661- 1662. Dash, M.C. & Dash, S.P. (2009). Fundamentals of Ecology. Tata McGraw Hill Publishing Company Ltd, N. Delhi, pp. 43-229. Engelmann, H.D. (1973). Undersuchangen zur Erfassung Pedozoogener component in difinicten okosystem, Forschungober, Staatl. Mus. Naturkde, Gorlitz. J. Acta Hydrobiol., 23(4): 349-361. Walkley, A. & Black, I.A. (1934). Determination of organic carbon in Soil. Soil Science, 37: 29-38. Gonzalez, G., Zou, X. & Boges, S. (1996). Earthworm abundance and species composition in abandoned tropical croplands: comparison of tree plantations and secondary forests. Pedobiologia, 40: 385-391. Shakir, S.H. & Dindal, D.L. (1997). Density and biomass of earthworms in forest and herbaceous microecosystems in central New York, North America. Soil Biology and Biochemistry, 29: 275-85. Hubers, H., Borges, S. & Alfaro, M. (2003). The oligochaetofauna of the Nipe soils in the Maricao State Forest, Puerto Rico. Pedobiologia, 47: 475-478. Sims, R.W. & Gerard, B.M. (1985). Synopses of the British Fauna (Eds. Kermack, D.M. and Barnes, R.S.K.) Earthworms, The Linnaean Society of London and the Estuarine and Brackish-Water Science Association, Breat Britain, p 124. Gates, G.E. (1972). Burmese Earthworms: An introduction to the systematics and biology of Megadrile Oligochaetes with special reference to Southeast Asia. Trans. Am. Phil. Soc. 62(7): 1-326. Julka, J.M. & Paliwal, R. (2005). Diversity and biogeography of Indian Earthworms. In: Proceedings of the UGC sponsored National Level Workshop on Vermitechnology, (Eds. Jeyaraaj, R. and Jayraaj, I.A.), Kongunadu Arts and Science College, Coimbatore, Tamil Nadu pp. 5-20. Shen, H.P. & Yeo, D.C.J. (2005). Terrestrial earthworms (Oligochaeta) from Singapore. The Raffles Bulletin of Zoology, 53(1): 13-33. Sarlo, M. (2006). Individual tree species effects on earthworm biomass in a tropical plantation in panama. Caribbean Journal of Science, 42(3): 419-427. Lapied, E. & Lavelle, P. (2003). The peregrine earthworm Pontoscolex corethrurus in the east coast of Costa Rica. Pedobiologia, 47: 471-474. Blanchart, E. & Julka, J.M. (1997). Influence of forest disturbance on earthworm (Oligochaeta) communities in the western ghats (South India). Soil Biology and Biochemistry, 29: 303-306. Fragoso, C. & Lavelle, P. (1987). On Earthworms (Eds. Bonvincini Pagliai, A.M. and Omodeo, P.), Mucci, Modena, Italy. pp 281-295. Gilot, C., Lavelle, P., Blanchart, E., Keli, J., Kouassi, P. & Guillaume, G. (1995). Biological activity of soil under rubber plantations in Cote dIvoire. Acta Zoologica Fennica, 196: 186-189. Bhadauria, T., Ramakrishnan P.S. & Srivastava, K.N. (2000). Diversity and distribution of endemic and exotic earthworms in natural and regenerating ecosystems in the central Himalayas, India. Soil Biology and Biochemistry, 32: 2045-2054. Kalisz, P.J. (1991). Native and exotic earthworms in deciduous forest soils of eastern North America. In: Proceedings of symposium on Biological Pollution: the control and impact of invasive exotic species, Indiana University Purdue University, Indianapolis pp. 93-100. Stern, H.J. (1967). Rubber: Natural & Synthetic. Maclaren and Sons Ltd. London.

[8] [9] [10] [11] [12] [13] [14] [15] [16] [17]

[18] [19]

[20] [21] [22] [23] [24] [25] [26]

[27]

[28]

368

Human-induced Biological Invasions in Rubber Plantations of Tripura

Nath & Chaudhuri

[29]

[30] [31] [32] [33]

Chaudhuri. P.S., Pal, T.K., Bhattacharjee, G. & Dey, S.K. (2003). Rubber leaf litters (Hevea brasiliensis var RRM 600) as vermiculture substrate for epigeic earthworm, Perionyx excavatus, Eudrilus eugeniae and Eisenia fetida. Pedobiologia, 47: 796-800. Kalisz, P.J. & Wood, H.B. (1995). Native and exotic earthworms in wild land ecosystems. In: Earthworm Ecology and Biogeography in North America, (Ed. Hendrix, P.F.), Lewis Publishers, Boca Raton, Florida pp. 117-126. Bhattacharjee, G. & Chaudhuri, P.S. (2002). Cocoon production, morphology, hatching pattern and fecundity in seven tropical earthworm species a laboratory based investigation. Journal of Bioscience, 27(3): 283-294. Pianka, E.R. (1970). On r and k selection. American Naturalist, 104: 459-466. Chaudhuri, P.S. & Bhattacharjee, S. (2009). Reproductive biology of eight tropical earthworm species of rubber plantations in Tripura, India. Tropical Ecology, 2009 (In Press).

369