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:: Volume 33, Issue 4 (10-2024) ::
isfj 2024, 33(4): 71-88 Back to browse issues page
Study of the distribution and density of Stylodrilus heringianus (Annelida: Lumbriculidae) along Cheshmehkileh and Sardabroud estuaries in Mazandaran Province (South Caspian Sea)
Meysam Erfani1 , Maryam Eslami2
1- Coldwater Fishes Research Center (CFRC), Iranian Fisheries Science Research Institute (IFSRI), Agricultural Research Education and Extension Organization (AREEO), Tonekabon, Iran.
2- Department of Microbiology, Faculty of Biotechnology, Islamic Azad University Qaemshahr branch, Qaemshahr, Iran.
Abstract:   (456 Views)
Introduction
Aquatic oligochaetes are members of a main group of macroinvertebrates and include about 1,700 species (Caramelo and Martinez-Ansemil, 2012) of 13 families with worldwide distribution (Martin et al., 2008). These species commonly inhabit within sediments of rivers, streams, lakes, marshes, ponds, springs and ground-waters (Collado and Schmelz, 2001), showing that these species have been adapted to a wide variety of habitats and environments, such as freshwater, brackish or seawater.
The freshwater oligochaete genus Stylodrilus is a large and heterogeneous. Although the genus has a Holarctic distribution, approximately 28, are exclusive to the Palaearctic region (Martin et al., 2007), except Stylodrilus heringianus a peregrine species recorded in the Australasian region and assumed to have been introduced by shipping (Brinkhurst & Jamieson, 1971).
From the Lumbriculidae family, only two species, L. variegatus and S. heringianus, have cosmopolitan, asexual reproduction (fragmentation) and use as live food in fish farming are the most important factors that have contributed to the distribution of these two species in the world (Pinder and Brinkhurst, 1994).
Cheshmehkileh of Tonekabon and Sardabroud of Chalus Rivers are the most important, mountainous and permanent rivers running from high elevation to the sea (southern waters of Caspian Sea). These rivers are important for reproductive migration of two indigenous valuable fisheries species Salmo caspius (Caspian trout) and Rutilus frisii (Caspian Kutum) as well as other migratory fish (Khara, 2016). For these reasons, estuary of these rivers is regarded as a ‘Protected Area’ and is conserved by the Department of Environment of Iran (DOE, 1996). 26 species of aquatic oligochaetes have been reported from inland waters of Iran so far, of which only 1 species belongs to the Lumbriculidae family and from Lumbriculus genus: L. variegatus (Ahmadi et al., 2012; Basim et al., 2012).  The aim of this study was to introduce Stylodrilus heringianus from Cheshmehkileh of Tonekabon and Sardabroud of Chalus Rivers in the Southern Caspian Sea basin for the first time and investigation of its distribution pattern in the three ecosystems of river, estuary and marine combined with some environmental factors in water (temperature and salinity) and sediment (grain size and total organic matter).
Methodology
Sampling of oligochaetes and environmental factors in both Sardabroud and Cheshmekile rivers, was carried out between November 2014 and September 2015 and random sampling was done at six stations with three replicates for each bimonthly sampling along each river. Sampling was done using 0.03 m2 Van Veen grab for soft sediments at the estuary area and for sampling at inner parts of the river with pebbles a 0.1 m2 and 0.2 mm-mesh size Surber sampler was applied. Biotic samples were fixed in situ using a 5% formalin solution. In the laboratory, sediments were sieved through mesh sizes of 1, 0.5 and 0.25 mm and specimens were preserved in 70% ethanol and then sorted and counted under a stereomicroscope (Nikon SMZ800, Japan) and eventually the wet weight of worms was measured using a digital balance (0.0001 g). For identification at species level, worm specimens were mounted on glass slides in Amman’s lactophenol clearing agent (Smith, 2001) and covered by a coverslip and left for several hours to a day or two, and then for observation of setae and other details, a microscope was used (Nikon E200). The main identification keys used were: Brinkhurst (1971a and b, Brinkhurst and Wetzel (1984), Brinkhurst (1986), Pinder and Brinkhurst (1994), Smith (2001), Arslan and Sahin (2003), Krieger and Stearns (2010), and Pinder (2010). In this study environmental variables, such as temperature and salinity in water were measured in situ by multimeter portable HACH-HQ40d model, and organic matter content was measured by the weight lost during ashing (Wildsmith et al., 2011), and grain size was analyzed by dry mechanical separation through a column of standard sieves of different mesh sizes, corresponding to classes described by Wentworth.
Results
In this study, the annual average water temperature was 18.2±0.2ºC. The average water temperature showed a significant difference between the sampling months (P<0.05), so that the lowest average water temperature were recorded in March as 10.1±0.08ºC and the highest in July as 30±0.8ºC. In both studied rivers, station (S1) has the lowest annual average salinity (0 g/l), station (S2) has average salinity in moderate level (6.7±1.2 g/l), and station (S3) has the highest annual average salinity (10.6±0.05 g/l). In both studied rivers, the average water salinity between sampling stations and months showed a significantly different (P<0.05), so that in station (S2), the highest average salinity was in July (8.3±1.5 g/l) and its lowest in January (5±0.8 g/l) and in station (S3) the highest average salinity in July (11.6±0.06 g/l) and its lowest in March (9.2±0.04 g/l) was recorded (Fig. 1).
The systematic account and description for the described species is as follows:
Kingdom: Animalia ; Phylum: Annelida Linnaeus, 1758 ; Class: Clitellata Linnaeus, 1740 ;  Subclass: Oligochaeta Grube, 1850 ; Order: Lumbriculida Claus, 1872 ; Family: Lumbriculidae Claus, 1872 ; Genus: Stylodrilus Claparède, 1862 ; Species: heringianus Claparède, 1862


Figure 1: Locality of sampling stations in studied transects (Google Earth, 2014-2015).  (S1: River, S2: Estuary, S3: Marine)
 Worms are olive gray or dark yellow with brown spots (Fig. 2A). Prostomium is without proboscis and most specimens have no eyes (Fig. 2B). Worms's body length was 23 to 69 mm and 0.5 to 1.3 mm in diameter with 28-71 segments. Dorsal and Ventral chaetae beginning in segment II and have 2 chaetae per bundle and 8 chaetae per segments (Fig. 2C). Chaetae in the anterior segments were simple pointed (Fig. 2D) and the posterior segments, bifid with upper tooth very short and reduced (Fig. 2E, F), with 35-55 μm long. A pair of penes on ventral side of X segment were visible in mature individuals (Fig. 2G).

Figure 2: Comparison of average (± standard deviation) of water temperature in sampling stations and months in studied transects, (S1: River, S2: Estuary, S3: Marine). Different letters indicate significant differences among averages (p<0.05).
In total, 40 individuals of S. heringianus were examined. During the present study, this species occurred in stations 1 (river) but was absent in station 2 (estuary) and 3 (marine) in both sampling areas. Density and biomass of this species among sampling months and stations were significantly different (p<0.05), as the highest average density and biomass were observed in Cheshmehkileh (station 1) in January (78±32.6 ind m-2 and 197±70 mg m-2), and the lowest of those were observed in Sardabroud (station 1) in September (9.7±4.3 ind m-2 and 18±7 mg m-2) respectively. Spatial distribution of S. heringianus among sampling stations (S1, S2 and S3) showed significant differences (p<0.05). In freshwater stations (S1) within the river average density and biomass were 42.6±17.3 ind m-2 and 113.3±40.3 mg m-2 respectively, and no specimens were observed in the estuary and marine stations (Fig. 3). In other words, no specimens were observed in the estuary (S2) and marine (S3) stations of both studied transects in all the sampling months (Table 1).

Figure 3: Comparison of average (± standard deviation) of water salinity in sampling stations and months in studied transects, (S1: River, S2: Estuary, S3: Marine). Different letters indicate significant differences among averages (p<0.05).

Table 1: characteristics and geographic locations of sampling stations in studied transects (S1: River, S2: Estuary, S3: Marine)
Transect Station Latitude (N) Longitude (E) Water type Sampling location Substratum nature Average depth (m)
Cheshmehkileh S1 N 36˚ 41' 11.9" E 51˚ 23' 55.4" Freshwater River Gravel, Sand, Silt, Clay, Vegetation 0.45
S2 N 36˚ 41' 22.2" E 51˚ 24' 8.7" Semi-brackish Estuary Gravel, Sand, Silt 0.86
S3 N 36˚ 41' 39.9" E 51˚ 24' 26.3" Brackish Marine Sand, Silt, Clay 7.08
Sardabroud S1 N 36˚ 49' 6.3" E 50˚ 52' 52.3" Freshwater River Gravel, Sand, Silt, Clay, Vegetation 0.5
S2 N 36˚ 49' 20" E 50˚ 53' 9.3" Semi-brackish Estuary Gravel, Sand, Silt 0.88
S3 N 36˚ 49' 35.9" E 50˚ 53' 24.6" Brackish Marine Sand, Silt, Clay 8.08
Temporal distribution of this worm in both studied transects showed significantly different among sampling months (p<0.05), as the highest average density and biomass of this species were observed in January as 58.6±23.7 ind m-2 and 175±55 mg m-2, respectively. While, the lowest of those values were in September as 9.7±4.3 ind m-2 and 18±7 mg m-2 (Fig. 4).


Figure 4: Comparison of average (± standard deviation) of sediment TOM percentage in sampling stations and months in studied transects, (S1: River, S2: Estuary, S3: Marine). Different letters indicate significant differences among averages (p<0.05).
A significant correlation (p<0.05) between density and biomass of S. heringianus with environmental variables was found (Table 2). A positive correlation was found between this species and gravel, silt and clay, while its correlations with temperature, salinity, TOM and sand were negative.
Table 2: Average of sediment grain size percentage in sampling stations and months in studied transects. (S1: River, S2: Estuary, S3: Marine)
Transect Month Gravel Sand Silt Clay
S1 S2 S3 S1 S2 S3 S1 S2 S3 S1 S2 S3



Cheshmehkileh
November 36.5 30.8 0 46.6 63.4 84 11.4 4 9.7 5.2 1.6 6.2
January 35.5 35.4 0 53.5 57.1 84 7.2 4.6 10.7 3.7 2.8 5.2
March 33.8 28.7 0 47.7 60.6 75.7 11.1 7.3 16.4 7.4 3.2 7.6
May 21.7 18.5 0 60.4 75 77.3 11.6 4.2 14.2 6.3 2.2 8.4
July 0.03 0.06 0 73.2 86.2 42.8 18.4 9 38.4 8.3 4.7 18.7
September 13.8 9.8 0 60.2 75 79.7 16.5 11.3 12.8 9.4 3.9 7.4



Sardabroud
November 7.1 32.4 0 66.4 61.8 79.7 17.3 3.4 14.2 9.2 1.8 5.8
January 21.8 14.8 0 56.2 77.5 85.2 15 5 9.3 6.8 2.7 5.3
March 17.3 28.9 0 53 59.5 73.2 18.1 7.6 19.1 11.5 3.8 7.6
May 14.6 23.1 0 70.2 69.2 76.6 10.1 5.2 14 5 2.4 9.5
July 4 21.6 0 63.1 73.3 86.4 22.6 3.7 9.3 2.1 1.3 4.2
September 6.4 18.8 0 59.6 72.4 79 21.7 5.7 13.6 12.1 2.9 7.3
Discussion and conclusion 
This study aims was done to identify and determine the distribution and density of Stylodrilus heringianus in Cheshmehkileh and Sardabroud river and estuary, alongside Iranian coasts and has not been previously reported from Iran’s freshwater fauna and Southern Caspian Sea basin. According to the taxonomic and morphological studies of the samples and the use of valid identification keys, and also sending photos of the samples to experts to confirm the identified species, it was determined that the samples belong to S. heringianus species. This species was recorded for the first time from Iran. This paper updated a short checklist of Iranian aquatic oligochaetes to 27 species (for Lumbriculidae to 2 species and for Stylodrilus genus to 1 species). In Table 3, the identified species of Lumbriculidae from Iran until now are listed and S. heringianus was not on the list.
Table 3: Density (ind/m2) and biomass (mg/m2) changes (average ± standard deviation) of S. heringianus in sampling stations and months in studied transects. (S1: River, S2: Estuary, S3: Marine)
Month Cheshmehkileh Sardabroud
S1 S2 S3 S1 S2 S3
November Density 11.7 A± 29.3 cd - - - - -
Biomass 30 A± 70d - - - - -
January Density 32.6 A± 78a - - 14.8 B± 39a - -
Biomass 70 A±a 197a - - 40 B± 91b - -
March Density 21.5 A± 48.8bc - - 23.8 A± 58.5a - -
Biomass 50 A± 163c - - 60 A± 188a - -
May Density 26.8 A± 68.3ab - - 15.2 B± 39a - -
Biomass 60 A± 183ac - - 40 B± 88b - -
July Density 8.2 A± 19.5d - - - - -
Biomass 10 A± 39d - - - - -
September Density - - - 4.3 A± 9.7b - -
Biomass - - - 7A± 18c - -
Annual average Density 20.1 A±48.8 - - 14.5 A±36.5 - -
Biomass 44 A±130.4 - - 36.7 B±96.2 - -
Different letters indicate significant differences among averages (p<0.05). Capital letters indicate variation among stations (horizontal), small letters indicate variation among months (vertical).
According to the results of this study, the highest average density and biomass of this species was observed in the cold months of the year (January and March) and the lowest in the warm months of the year (July and September), whereas density and biomass of this species show a significant negative correlation with water temperature, that this increase in density can be due to the asexual reproduction of Architomy and Parathomy (Smith, 2001) of this species in the cold months of the year, and its reduction in the warm months of the year (July and September) can probably be related to the feeding of fish with this worm. In the present study, S. heringianus was observed only in the river's freshwater ecosystem (salinity 0 ppt) and it was not observed in both estuarine brackish ecosystems with a salinity range of 5 to 8 g/l and marine brackish ecosystem with a salinity range of 9 to 11.5 g/l, which indicating that this species is oligohaline (does not tolerate salinity more than 1 g/l). Considering that the sediments grain size and the percentage of total organic matter were almost the same in the both ecosystems of river freshwater and estuarine brackish, it can be concluded that the limiting factor for distribution of this species in the estuarine and marine environments, maybe it is because of salinity intolerance, even to a very low level.
Substrates in both rivers at Freshwater sampling stations (S1) were covered with vegetation in littoral and some central zone, but substrates in estuary and marine brackish stations (S2 and S3) vegetation cover was absent, According to the results of other researchers' studies about dependency of this species to vegetation habitats, probably, the main reason of density and biomass increase of this species in freshwater sampling stations was presence of vegetation habitats and its decrease in brackish water stations was due to absence of this habitat. Possibly, for this is reason, S. heringianus showed significant negative correlation with salinity. Among the investigated environmental factors, temperature and salinity of water and sand have the most influence on the distribution of this species. In addition to its important role in the food chain of water resources, this species is also considered as a bioindicator of water quality and is used as live feed in the aquaculture industry.
Keywords: First record, Stylodrilus heringianus, Cheshmehkileh, Sardabroud, Caspian Sea
Full-Text [PDF 1035 kb]   (181 Downloads)    
Type of Study: Research | Subject: اكولوژي محيطهاي آبي
Received: 2024/03/24 | Accepted: 2024/10/31 | Published: 2024/12/23
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Erfani M, Eslami M. Study of the distribution and density of Stylodrilus heringianus (Annelida: Lumbriculidae) along Cheshmehkileh and Sardabroud estuaries in Mazandaran Province (South Caspian Sea). isfj 2024; 33 (4) :71-88
URL: http://isfj.ir/article-1-2795-en.html


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Volume 33, Issue 4 (10-2024) Back to browse issues page

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