First record of Limnodrilus claparedeianus Ratzel, 1868 (Annelida: Oligochaeta: Tubificidae) in Anzali Wetland, Guilan province, Iran

Authors

1 Islamic Azad University Science and Research Branch of Tehran

2 Islamic Azad University North branch of Tehran

3 University of Guilan

4 Islamic Azad University Science and Research Branch of Tehran,

Abstract

Oligochaeta worms are important organisms in aquatic ecosystem. Their omnipresence makes them as an indicator of environmental changes and health of aquatic ecosystem. The members of the family Tubificidae and in particular, genus Limnodrilus are considered as the most tolerant oligochaets to aquatic pollution. Therefore identification and biological characteristics of this taxon are of great help to evaluate the ecosystem of water bodies. Limnodrilus claparedeianus were collected from Anzali Wetland with a grab of 0.04 m2 capacity at 13 stations from August 2012 through June 2013. Penis sheath was one of the main characteristics to identify them. Results showed their maximum and the minimum density in spring (601.27±  466.8346 Ind.m-2) and in autumn (156.12 ±136.3Ind.m-2) respectively which was significantly different (P<0.05). Comparative spatial distribution of L. claparedeianus among 13 stations revealed significant differences in the west stations (P<0.05). According to the results, correlation analysis did not exhibit any relation between abundance of L. claparedeianus and total organic matter, abundance of the species and percentage of silt in substrate sediment.

Keywords


[Short Communication]

First record of Limnodrilus claparedeianus Ratzel, 1868 (Annelida: Oligochaeta: Tubificidae) in Anzali Wetland, Guilan province, Iran

 

F. Nazarhaghighi1, R. Mousavi Nadoushan2, N. Shabanipour*3, M. R. Fatemi1, A. Mashinchian Moradi1

1. Dept. of Marine Biology, Graduate School of Marine Science and Technology Islamic Azad University, Science and Research Branch, Tehran, Iran.

2. Faculty of Marine Science & Technology, Islamic Azad University, North branch, Tehran, Iran.

3. Faculty of science, University of Guilan, Rasht, Iran.

* Corresponding author’s E-mail: shabani@guilan.ac.ir

(Received: Dec. 30.2014 Accepted: May. 27.2015)

ABSTRACT

Oligochaeta worms are important organisms in aquatic ecosystem. Their omnipresence makes them as an indicator of environmental changes and health of aquatic ecosystem. The members of the family Tubificidae and in particular, genus Limnodrilus are considered as the most tolerant oligochaets to aquatic pollution. Therefore identification and biological characteristics of this taxon are of great help to evaluate the ecosystem of water bodies. Limnodrilus claparedeianus were collected from Anzali Wetland with a grab of 0.04 m2 capacity at 13 stations from August 2012 through June 2013. Penis sheath was one of the main characteristics to identify them. Results showed their maximum and the minimum density in spring (601.27±  466.8346 Ind.m-2) and in autumn (156.12 ±136.3Ind.m-2) respectively which was significantly different (P<0.05). Comparative spatial distribution of L. claparedeianus among 13 stations revealed significant differences in the west stations (P<0.05). According to the results, correlation analysis did not exhibit any relation between abundance of L. claparedeianus and total organic matter, abundance of the species and percentage of silt in substrate sediment.

Key words: Anzali Wetland, Limnodrilus claparedeianus, new record.


INTRODUCTION

Benthic macro-invertebrate communities in wetlands are important component of the aquatic environment which plays momentous roles in the energy pathway and nutrient cycling, assessment of the ecological entirety and bio-monitoring of aquatic habitats (Lae, 1994; Gordon, 2000; Acharyya & Mitsch, 2001; MRC, 2010). They also establish an important connection as food reservoir for fishes and other animals in aquatic food chain (Blay & Dongdem, 1996; Arslan et al., 2007). Among benthic communities, oligochaetes are common and abundant animal groups, which are strongly influenced by environmental conditions. Out of more than 5000 known species of class Oligochaeta, approximately 1100 species live in freshwater (Suriani et al., 2007). Environmental richness of oligochaete species is directly related to food availability and quality, substrate type, oxygen availability and biological interactions. Furthermore this group are not much motile and mostly are considered as indicators of specific trophic state of aquatic habitat (Behrend et al., 2012). Generally, oligochaetes have wide geographical distribution patterns and their population can sometimes reach quite large number. Many species prefer eutrophic water, living on muddy sediments with abundant detritus organic matter. Anzali Wetland is an internationally known inland water body in north of Iran and has gained more reputations as being connected to Caspian Sea. It hosts a wide variety of animal species and therefore possesses great ecological concern to remain under continuous monitoring. The present study introduces Limnodrilus claparedeianus and its distributional peculiarities as a monitoring index.

 

MATERIALS AND METHODS

Study area

Anzali Wetland (37◦28_ N, 49◦25_ W) represents an internationally important wildlife reservoir and sanctuary with an open surface area of 58 km2 which is listed under Ramsar Convention (Pourang, et al. 2010) (Fig. 1). Urbanization and population growth, industrial and agricultural activities, and also tourism are major sources of pollutants discharged into the Wetland directly or via rivers indirectly.

 The southern part of the wetland is mainly under rice cultivation and patches of woodland, while the northern part is bordered by sand dunes, grassland and scrubby vegetation (Ayati, 2003).

 

Sampling and sample preparation

The specimens of Limnodrilus claparedeianus were collected seasonally from 13 stations in Anzali Wetland from August 2012 through June 2013 (Fig. 1 and Table. 1). The oligochaetes were collected with grab (0.04 m2) accompanied with bryophytes and other submerged plants and also from bottom surface layer.

The sediments were passed through a 500 μm mesh size sieves on spot and sieved particles were preserved in 10% formalin. In the laboratory, samples were then isolated and transferred to 70% ethanol.

Worm specimens were dipped in Amman’s lactophenol for transparency, mounted on microscope slides covered by a cover slip and left for several hours before examination.

All measurements and photographs for preserved specimens were taken and analyzed by TSVIEW 5 mega pixel camera and software (version 6.2.4.5).

Identifications followed detailed description made by Kathman and Brinkhurst (1998) and Douglas (2001).

Certain collected specimens during this study are now deposited in Dr. Tarmo Timm’s fresh water annelid collections, Centre for Limnology, Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences under code number S-4333.

Total organic matter of sediment and the granulometric analysis followed the procedures described by Moghaddasi et al. (2009).

 


 

Fig. 1. Study area and sampling sites.

 

 

 

 

Table 1.  Coordination of sampling sites.

Latitude

Longitude

Station

49 19 20

37 28 22

1

49 20 06

37 28 50

2

49 22 48

37 27 13

3

49 24 38

37 26 13

4

49 24 30

37 24 51

5

49 22 41

37 24 22

6

49 25 31

37 25 07

7

49 26 48

37 25 33

8

49 26 54

37 24 31

9

49 25 46

37 24 18

10

49 28 49

37 26 56

11

49 28 25

37 26 09

12

49 28 05

37 26 00

13


 

DATA ANALYSIS

Data analysis was done by SPSS version 18. Data normality was assessed using the Kolmogorov-Smirnov test.

For normally distributed data, One-Way ANOVA was performed. Otherwise, the Mann-Whitney U test and Kruskal -Wallis test was applied. For entry data to computer and calculation of mean, standard error, charting and other operations, Excel 2007 was used.

 

RESULTS

Morphological descriptions

Live specimens were red in color but formaldehyde preserved ones turned into milky cream. Worm body was 7 to 35 mm in length and 3 to 4 mm in diameter. The cylindrical body showed bilateral symmetry and at least 40 to more than 100 segments were

 

 

counted. Eye spots were absent. Caudal region was undifferentiated with conical prostomium (Fig. 2a, b). Dorsal and ventral chaetae commenced from second body segment, regularly and alternatively at upper and lower regions of body (Fig. 2d). All chaetae were bifid and similar, upper tooth longer than lower tooth or slightly equal and hair were absent in dorsal bundle (Fig. 2c). Anterior segments were comprised of 6-8 chaetae per dorsal bundle and 2 chaetae per ventral bundle. Clitellum was seen in segments X to XII. Like other oligochaets, L. claparedeianus was hermaphrodite where male and female organs appeared simultaneously over transparent body wall (Fig. 2a). Paired penial sheath distinguishable in segments XI was one of the main identifying characteristics (Fig. 2: a, g).

 

 

Table 2. Abundance (mean ± SD) of L. claparedeianus.

Spring

Winter

Autumn

Summer

season

station

53.33 ± 18.95

25.66 ± 19.68

____

___

S1

124 ± 25.5

_____

____

50 ± 44.72

S2

____

16.66 ± 12.9

____

86 ± 13.50

S3

53.28 ± 8.68

1485 ± 207.81

246.33 ± 78.34

236 ± 40.70

S4

862.66 ± 123.35

658.37 ± 66.59

226.67 ± 53.23

1139 ± 283.84

S5

1296.66 ± 292.51

138.23 ± 56.14

193 ± 51.71

581.66 ± 217.36

S6

456 ± 126.06

1303 ± 428.02

96.66 ± 34.97

536.33 ± 177.02

S7

991 ± 271.91

217.16 ± 59.3

358 ± 65.56

3062.33 ± 821.36

S8

925 ± 530.915

717 ± 267.5

154 ± 69.83

317.68 ± 54.08

S9

403 ± 193.19

266.66 ± 71.39

456 ± 192.35

522.66 ± 279.86

S10

484.66 ± 29.62

240 ± 60.42

105.36 ± 52.49

158.24 ± 87.91

S11

1389 ± 151.84

1216.33 ± 394.85

76.66 ± 32.67

239 ± 88.32

S12

778 ± 153.74

1068.25 ± 317.39

117 ± 28.41

623.66 ± 234.78

S13

 

Fig. 2. (a) Anterior end of L. claparedeianus, location of penial sheaths (arrow) and clitellum (ellipse). (b) Conical head region of L. claparedeianus. (c) Dorsal and ventral chaetae. (D) Location of dorsal (upper arrow) and ventral chaetae (lower arrow). (E, g) micrographs and (h, k) Schematic figures of penial sheath anterior end. (f) Penis (arrow) located within the transparent penial sheath.

 

Seasons

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 


Fig. 3. Seasonal mean abundance of L. claparedeianus.

 

Table 3. List of identified oligochaetes in Anzali Wetland (JICA, 2005).

references

Family:

Tubificidae

Family: Lumbriculidae

Family:

Naididae

Mirzaee Bafti,1991

Tubifex sp.

-

-

Abdolmaleki, 1993

Tubifex sp.

-

-

Khodaparast, 1996

Tubifex sp.

Vareigatus sp.

-

Mirzajani et al. 1999

Tubificidae

-

-

Ahmadi and Khara, 2006

Tubificidae

-

Naididae

Mirzajani et al. 2009

Tubificidae

Lumbriculidae

Naididae

JICA, 2005

Tubifex sp.

Lumbriculus sp.

Nais  sp.

Jalili et al. 2011

Tubifex sp.

Lumbriculus sp.

-

 

 

 
   
 

 

 

 

 

 

 

 

 

 

 


Fig. 4. Spatial mean abundance of L. claparedeianus

 

 

Stations

 
   
 

 

 

 

 

 

 

 

 

 

 

 

 

 


Fig. 5. Mean abundance of L. claparedeianus in 13 stations is compared in four seasons.

 

Table 3. List of identified oligochaetes in Anzali Wetland (JICA, 2005).

references

Family:

Tubificidae

Family: Lumbriculidae

Family:

Naididae

Mirzaee Bafti,1991

Tubifex sp.

-

-

Abdolmaleki, 1993

Tubifex sp.

-

-

Khodaparast, 1996

Tubifex sp.

Vareigatus sp.

-

Mirzajani et al. 1999

Tubificidae

-

-

Ahmadi and Khara, 2006

Tubificidae

-

Naididae

Mirzajani et al. 2009

Tubificidae

Lumbriculidae

Naididae

JICA, 2005

Tubifex sp.

Lumbriculus sp.

Nais  sp.

Jalili et al. 2011

Tubifex sp.

Lumbriculus sp.

-

 


Spatial and seasonal distribution patterns of L. claparedeianus

This species was observed in all seasons and within all mesohabitats. Statistical analysis was performed in order to determine the probability existence of spatial and seasonal patterns relating the abundance to certain physico-chemical parameters. A distinct seasonal maximal mean for abundance L. claparedeianus was observed in spring (601.27 ± 466.83 Ind.m-2) and minimum in autumn (156.12 ± 136.3 Ind.m-2). From spatial point of view the maximum abundance mean was observed in station 8 (e.g. Sorkhankol wild life refuge, 1157.12 ± 1216.49 Ind.m-2) and a minimum in western station 1 (19.74 ± 23.55 Ind. m-2) (table1). Seasonal density average was s comparatively significantly different only in autumn (P<0.05) (Fig. 3). Spatial distribution of L. claparedeianus in stations were compared using Kruskal-Wallis and Mann-Whitney U test, and lack of normal distribution of data was assessed by Kolmogorov-Smirnov test, revealing that the mean abundance of total population of the species among 13 stations was significantly different between western stations and other stations located at Siahkeshim (Southern part), Sorkhankol (central part) and eastern part of the Wetland, (P<0.05). Meanwhile, there was no significant difference among different stations of each part. According to the results obtained, correlation analysis did not detect any relations between abundance of L. claparedeianus and total organic matter, also between abundance of the species and percentage of silt in substrate sediment.

 

DISCUSSION AND CONCLUSION

During one year sampling in Anzali Wetland, L. claparedeianus was observed for the first time in Iran. Lack of eyes, terminal anus, undifferentiated caudal region, conical prostomium were clear characteristics to identify the Family. However some characters like the number of chaetae per bundle, the shape of the chaetae, availability, length and shape of penis sheath were also used. The upper tooth of chaetae was often longer than the lower one, but these chaetae in some specimens were difficult to distinguish from those of L. hoffmeisteri because the upper tooth was only slightly longer than the lower one. The most trusted reliable key to identify Limnodrilus genus at species level was the shape of penis sheath particularly the shape of distal end (Kennedy, 1969; Brinkhurst, 1971; Bird & Ladle, 1981; Ohtaka, 1985; Yasuda & Okino, 1987; Pinder & Brinkhurst, 1994; Swayne et al., 2004; Krieger & Stearns, 2010). It is worth noting that variations in the lengths of the oligochaete body, chaetae and the number of segments are common and suspected to be due to locality differences (Al-Abbad, 2012).  Harber (1938) and Sperber (1948) emphasized that these variations in length and number of segments occurred even within the same species.

In a general study (Table 2) 5 reported taxa represented five genera in three families in Anzali Wetland (JICA, 2005) and L. claparedeianus was not in the list. Constant observation of this species in all seasons and within all mesohabitats and different substrate of wetland can reveal the fact that the species is compatible to harsh environmental condition and various habitats. Maximum seasonal abundance mean of the L. claparedeianus in spring (601.27 ± 466.83 Ind. m-2) while minimum in autumn (156.12 ± 136.3 Ind.m-2) and nonexistent significant difference among other seasons could be due to optimum environmental condition (such as food availability and temperature) in spring. Stephan and Alves (2001) concluded that the high densities of Limnodrilus may suggest high amount of food availability (organic matter) together with rare opportunities for biotic interactions such as predation and competition. They are a consequence of water pollution which may play an important role in the fitness of such genus in Pedro stream. Studies on oligochaete species in the Scandinavian lakes based on the degree of enrichment indicated that L. claparedeianus belonged to a group of species tolerating extreme enrichment of organic pollution (Rodriguez & Reynoldson, 2011). On the other hand, research works have proven in recent years that water eutrophication has turned to be a serious environmental challenge to Anzali Wetland ecosystem as increasing waste loads from industrial, agricultural and human activities to international has reached an alarming level (Akbarzadeh et al., 2008; Mirzajani et al., 2010). Since members of the genus Limnodrilus are considered as one the most tolerant oligochaetes especially to organic pollutions (Brinkhurst, 1980; Milbrink, 1980; Lang, 1984; Seys et al., 1999), their continuous presence in Anzali Wetland might indicate existence of high degrees of organic pollution. It should be noted that classification of some aquatic oligochaetes like L. claparedeianus from the St. Lawrence Great lakes has placed the lake in eutrophic level (Rodriguez & Reynoldson 2011).

It can therefore be concluded that densely presence of L. claparedeianus in Anzali Wetland in all sampling sites and all seasons except autumn, illustrates high organic pollution load in all parts of the Wetland and also in most seasons.

The effect of organic pollutions could also be observed on wetland regional basis. For example, station 8 (Sorkhankol wild life refuge) located at the south of Anzali Wetland (1157.12 ± 1216.49 Ind.m-2) which provided the maximum L. claparedeianus density used to receive large amount of agricultural, urban wastewater, remains of plants and animals, while the least abundance of L. claparedeianus, was observed at stations located in the western part of the Wetland.

The western region met lower industrial and agricultural activities and therefore establishing a healthier environmental condition.  Anzali Wetland is a complex costal wetland and affected by many environmental parameters.

Suriani et al. (2007) stated the species composition, abundance and distribution of benthic invertebrates usually depended on many variables as important as the substrate type, dissolved oxygen concentration, water level fluctuation, biotic food quality and availability, competition and finally predation. In the present study, a correlation between abundance of L. claparedeianus and total organic matter and percentage of silt in substrate sediment was not observed. Yap et al. (2006) suggested non-existing correlation between abundance of Limnodrilus and total organic matter could indicate that this group is resistant to pollution, however detailed study and discussion on how abiotic factors influence the distribution of the resistant Limnodrilus sp. has not yet been discussed in the literature.

According to the results obtained through the present study it could be concluded that permanent presence of L. claparedeianus in highly TOM loaded (19.56 ± 7.04), Anzali Wetland is a warning sign which has to be considered seriously.

 

ACKNOWLEDGEMENT

The authors are grateful to Dr. TarmoTimm, Estonian University of Life Sciences for assistance in species identification.

Abdolmaleki, Sh, 1993, the annual analytical report of Anzali Wetland benthos. Joint project of Guilan Fisheries Research Organisation and FAO. (In Persian)

Acharyya, S & Mitsch, WJ, 2001, Macroinvertebrate diversity and its ecological implications in two created wetland ecosystems. In: WJ Mitsch; L Zhang. (Ed.), The Olentangy River Wetland Research Park at The Ohio State University Annual Report  2000The Ohio State University, Columbus, USA. pp 65-76.

Ahmadi, M & Khara, H, 2006, Limnological survey of Sorkhankol wild refuge. Final report presented to University of Tehran (research and technology assistance) and Department Of Environment of Guilan. 750pp. (In Persian)

Akbarzadeh, A, Laghai, H-A.Monavari, M, Nezami, SA, Shokrzadeh, M & Saeedi Saravi, SS, 2008, Survey and determination of Anzali wetland trophic state through geographic information systems (GIS). Toxicological & Environmental Chemistry 90(6): 1055 - 62.

Al-Abbad, MYM, 2012, New Records of twelve species of Oligochaeta (Naididae and Aeolosomatidae) from the Southern Iraqi Marshes, Iraq. J. JBS. 5(2): 105 – 111.

Arslan, N, lhan, Shahin, Y, Filik, C,  Yılmaz, V, & Öntürk, T, 2007, Diversity and distribution  of  benthic  invertebrates  community  structure  in relation  to  environmental  parameters  in  the  littoral  zone  of  Musaözü Dam Lake, Eskiehir. Journal of Applied Biological Science 1(3): 67-75.

Ayati, B, 2003, Investigation of sanitary and industrial wastewaters effects on Anzali Reserved Wetland. Final report presented to: MAB-UNESCO.

Behrend, RDL, Takeda, AM, Gomes, LC, Fernandes, SEP, 2012, using oligochaeta assemblages as an indicator of environmental changes. Brazilian Journal of Biology, 72(4): 873-884.

Bird, GJ, & Ladle, M, 1981, Aspects of the morphology and ecology of two British tubificids (Oligochaeta). Journal of Zoology London, 194: 493-504.

Bishel-Machung, L, Brooks, RP, Yates, SS, & Hoover, KL, 1996, Soil properties of reference wetlands and wetland creation projects in Pennsylvania. Wetlands. 16: 532–541.

Brinkhurst, R0, 1971, A guide for the identification of British aquatic Oligochaeta. Freshwater biological association. Scientific publication. No. 22. pp 55.Titus Wilson & Sons LTD. Kendal.

Brinkhurst, RO, 1980, Pollution biology of the North American experience. In R. O. Brinkhurst & D. G. Cook (eds.), Aquatic Oligochaete Biology. Plenum Press, New York. pp. 205–209.

Blay, J, Jr, & Dongdem, F, 1996, Preliminary observations on the benthic macrofauna of a polluted coastal lagoon in Ghana (West Africa). Tropical Ecology 37(1): 127-133.

Douglas GS, 2001, Pennak’s freshwater invertebrates of the United States. Porifera to Crustacea. Fourth edition, pp. 664. Johns Wiley & Sons.

Fabbrocini, A, Matteo, ODD’& Adamo, R, 2008, Abrasegmentum (Mollusca: Pelecypoda) of the Lesina Lagoon (Southern Adriatic coast, Italy): Observation to the main environmental parameters. T. W.  B., 1:39-44.

Gordon, C, 2000, Hypersaline lagoons as conservation habitats: macro-invertebrates at Muni Lagoon, Ghana. Biodivers. Conserv.9: 465-478.

Harber, S, 1938, Trichodrilus maravicus und Claparedei, Neue Lumbriculidae. Zool Anz.15 -73.

Jafari, N, 2009, Ecological integrity of wetland, their functions and sustainable use. Journal of Ecology in Natural Environment, 1 (3): 45-54. 

Japan International Cooperation Agency (JICA) 2005, the study on integrated management for ecosystem conservation of the Anzali Wetland in the Islamic Republic of Iran. Final report submitted to department of environment.

Jalili, M, Negarestan, H, Safaeeian, Sh, 2011, survey on macrobenthos of southwestern part of Anzali Wetland and its association with organic matter context. Oceanography, 1(4):11-20. (In Persian)

Kathman, RD, & Brinkhurst, RO, 1998, Guide to the freshwateroligochaetes of North America: College Grove, Tennessee, Aquatic Research Center.

Kennedy, CR, 1969, The variability of some charactersused for species recognition in the genus Limnodrilus (Oligochaeta :Tubificidae) . J ournal of Naural History, 3: 53-60.

Khodaparast, S, 1996, Comprehensive report of hydrology and hydrobiology project of Anzali Wetland. Guilan Fisheries Research Organization (In Persian)

Krieger, KA, & Stearns AM, 2010, Atlas of the Aquatic Oligochaete Worms (Phylum Annelida: Class Clitellata:  Superorder Microdrili) Recorded at the Old Woman Creek National Estuarine Research Reserve and State Nature Preserve. Pp. 32. Ohio National Center for Water Quality Research Heidelberg University Tiffin, Ohio, USA.

Laë, R, 1994, Evolution des peuplements (poissonset crustacés) dansunelagune tropicale, le lac Togo, soumise à UN régime alternatif de fermeture ET d’ouverture du cordon lagunaire. Aquatic Living Resources, 7:165-179.

Lang, C, 1984, Eutrophication of Lakes Léman and Neuchâtel (Switzerland) indicated by oligochaete communities. Hydrobi,ologia, 115: 131–138.

Mekong River Commission,Vientiane (MRC). 2010, Biomonitoring Methods for the Lower Mekong Basin. 65 pp.

Milbrink, G, 1980, Oligochaete communities in pollution biology: the European situation with special reference to lakes in Scandinavia. In R. O. Brinkhurst & D. G. Cook (eds.), Aquatic Oligochaete Biology. pp. 433–455. Plenum Press, New York.

Mirzaee Bafti, A, 1991, Survey of benthos of Anzali Wetland and rivers radiating from it. Iranian Fisheries Research Organization (In Persian)

Mirzajani, A, Yousefzadeh, A & Ghanea, A, 1999, Benthic invertebrates and their relationship with the organic material in the context of Anzali Lagoon. Iranian Journal of Fisheries Science, 7(4): 83-102. (In Persian).

Mirzajani, A, 2009, Limnological survey of Anzali Wetland Based on 1992-2002 GIS data (1991-2001). Iranian Fisheries Research Organization (In Persian)

Mirzajani, AR, Khodaparastsharifi, H, Babaei, H, Abedini, A, DadaiGhandi, A, 2010, Eutrophication Trend of Anzali Wetland Based on 1992-2002 Data.  Journal of Environmental Studies, 35(52): 19-21.

Moghaddasi, B, Nabavi, SMB, Vosoughi, G, Fatemi, SMR, & Jamili, S, 2009, Abundance and Distribution of Benthic Foraminifera in the Northern Oman Sea (Iranian Side) Continental Shelf Sediments Research. Journal of Environmental Sciences Acad. 2: 210-217.

Nazarova, L,       Semenov, B,        Sabirov, VF,         Efimov, RM,        Yu, I, 2004, the state of benthic communities           and water quality evaluation in the        Cheboksary         Reservoir. Water Resource Bulletin 31(3): 316–322.

Ohtaka, A, 1985, Taxonomical revision of three Japanese Limnodrilus species (Oligochaeta, Tubificidae). Proceeding of Japanese .Society Systematic Zoology, 30: 18-34.

Pinder AM, & Brinkhurst R. 1994, a preliminary guide to the identification of the microdrile oligochaeta of Australian inland waters. pp 144.Cooperative research center for freshwater ecology, Albury.

Pourang, N, Richardson, CA, Mortazavi, MS, 2010, Heavy metal concentrations in the soft tissues of swan mussel (Anodontacygnea) and surficial sediments from Anzali Wetland, Iran. Environ. Monit. Assess. 163:195–213.

Rodriguez, P & Reynoldson, TB, 2011, the Pollution Biology of Aquatic Oligochaetes. Pp. 265. © Springer Science Business Media B.V.

Seys, J, Vincx, M & Meire, P, 1999, spatial distribution of oligochaetes (Clitellata) in the tidal freshwater and brackish parts of the Schelde estuary (Belgium). Hydrobiologia, 406:119–132.

Sperber, C, 1948, A taxonomical study of the Naididae. Zool. Bidrag. Uppsala. 28: 1-296.

Stephan, MR, & Alves, RG, 2008, Tubificidae (Annelida: Oligochaeta) as an indicator of water quality in an urban stream in southeast Brazil. Tubificidae (Annelida: Oligochaeta) comoindicador da qualidade da água de um córregourbano do sudeste Brasileiro. Acta Limnologica Brasilia 20(3): 221-226.

Suriani, AL, Franca, RS, Pamplin, PAZ, Marchese, M, Lucca, JV, & Rocha, O, 2007, Species richness and distribution of oligochaetes in six reservoirs on Middle and Low Tiete river (SP, Brazil). Acta Limnologica Brasilia 19(4): 415-426.

Swayne, H, Day, M & Wetzel, MJ, 2004, Limnodrilus hoffmeisteri (Annelida: Oligochaeta: Tubificidae) in Pop’s Cave, Wisconsin, USA. J. Cave Karst Stud. 66 (1):28-31.

Yap, CK, Rahim Ismail, A, Azrina, MZ, Ismail, A, Tan, SG, 2006, the influential of physico-chemical parameters on the distributions of oligochaetes (Limnodrilus sp.) at the polluted downstream of the tropical Langat River, Peninsular Malaysia. Journal of Applied Science, Environmental Management 10(3):135-140.

Yasuda, K & Okino, T, 1987, Distribution and seasonal changes of aquatic Oligochaeta in Lake Suwa. Japanese Journal of Limnology 48: 1-8.