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Nematode community structure in relation to metals in the southern of Caspian Sea
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Bastami Kazem Darvish1, *, Taheri Mehrshad1, Foshtomi Maryam Yazdani1, Haghparast Sarah2, Hamzehpour Ali1, Bagheri Hossein1, Esmaeilzadeh Marjan3, Molamohyeddin Neda4
Acta Oceanologica Sinica | 2017, 36(10) : 79 - 86
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Acta Oceanologica Sinica | 2017, 36(10): 79-86
• •
Nematode community structure in relation to metals in the southern of Caspian Sea
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Bastami Kazem Darvish1, *, Taheri Mehrshad1, Foshtomi Maryam Yazdani1, Haghparast Sarah2, Hamzehpour Ali1, Bagheri Hossein1, Esmaeilzadeh Marjan3, Molamohyeddin Neda4
Affiliations
  • 1 Iranian National Institute for Oceanography and Atmospheric Science (INIOAS), Tehran 1411813389, Iran
  • 2 Department of Fisheries, Faculty of Animal Science and Fisheries, Sari Agricultural Sciences and Natural Resources University, Sari 578, Iran
  • 3 Department of Environmental Science, Faculty of Environment and Energy, Science and Research Branch, Islamic Azad University, Tehran 1477893855, Iran
  • 4 Department of Marine Science and Technology, Tehran North Branch, Islamic Azad University, Tehran 1477893855, Iran
Published: 2017-10-01 doi: 10.1007/s13131-017-1051-x
Outline
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Spatial distribution and structure of nematode assemblages in coastal sediments of the southern part of the Caspian Sea were studied in relation to environmental factors. By considering metals, organic matter, Shannon diversity index (H), maturity index (MI) and trophic diversity (ITD), ecological quality status of sediment was also determined. Fifteen nematode species belonging to eleven genera were identified at the sampling sites. Average density of nematode inhabiting in sediment of the studied area was 139.78±98.91 (ind. per 15.20 cm2). According to redundancy analysis (RDA), there was high correlation between metals and some species. Based on biological indicators, the studied area had different environmental quality. Generally, chemical and biological indices showed different results while biological indices displayed similar results in more sites.

free-living nematodes  /  metal  /  ecological quality status  /  the Caspian Sea
Bastami Kazem Darvish, Taheri Mehrshad, Foshtomi Maryam Yazdani, Haghparast Sarah, Hamzehpour Ali, Bagheri Hossein, Esmaeilzadeh Marjan, Molamohyeddin Neda. Nematode community structure in relation to metals in the southern of Caspian Sea[J]. Acta Oceanologica Sinica, 2017 , 36 (10) : 79 -86 . DOI: 10.1007/s13131-017-1051-x
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1 Introduction
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The Caspian Sea, which regards as 40% to 44% of the total lacustrine waters of the world, is still under debate to be ascribed as a sea or a lake. Owing to high biodiversity, the sea is regarded as one of the most valuable ecosystems on the earth. The Caspian Sea, as a closed water body, has a high level of endemism which is remarkably evident in its fauna. Various features of the sea, such as the presence of shallow areas, several deep depressions and a wide range of salinities from 0.1‰ to 13‰ offer different ecological niches which give rise to high species diversity.
In most marine meiobenthic habitats, nematodes are numerically the dominant animal group and have wide distribution, inhabiting in pristine to extremely polluted habitats. Usually, 70%–90% of the meiobenthic metazoan abundance is dedicated to nematodes in marine sediments, where they play major ecological functions (Austen, 2004).
Nematodes, with a daily and/or weekly generation time, represent high density and continuous reproduction all over the year (Austen and McEvoy, 1997). The highly abundance and diversity of nematodes, in addition to their wide distribution often provide more strong data than what can be acquired for most larger-sized organisms (review by Heip et al., 1985; Bongers and van de Haar, 1990; Leduc et al., 2015).
Biological activities of nematodes like as absorption of dissolved organic compounds, consumption of fungi and other organisms, nutrients regeneration, changes in sediment texture by mucus secretion, improvement of gas diffusion as well as serving as a food source for other predators from their own taxon make their presence essential within the benthic network of organisms (Bongers and van de Haar, 1990; Taheri et al., 2015).
Until now, although many researchers have focused on the ecology and biodiversity of the nematodes in many parts of the world (e.g., Heip et al., 1985; Giere, 2009; Gambi and Danovaro, 2016), their species richness especially in less investigated coastal areas such as the Caspian Sea is still unknown.
Only a few studies have described nematodes in the Caspian Sea (Zenkevich, 1963; Birshtein et al., 1968; Chesunov, 1980; Tchesunov, 1981) especially in the southern part in Iranian border (Riyazi, 2002; Mirzajani et al., 2003).
The objective of this study was to investigate the composition of the nematode community from the southern part of Caspian Sea, and to evaluate the correlations between nematode abundance, composition and distribution and the main environmental contaminants.
2 Materials and methods
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2.1 Nematode sampling and identification
Sampling was conducted in six shallow water stations (Fig. 1) with different sediment types and depth ranged from 7 m to 15 m in autumn (November 2013). At each sampling location, three replications of the cores (id=4.4 cm) were collected to a depth of 4 cm. Samples were then fixed in 4% neutral formaldehyde seawater solution in different containers.
Each sample after transferring to the laboratory was firstly sieved through a 1-mm and then a 38-μm mesh size sieve. Thereafter, the remaining fraction was centrifuged three times with Ludox (colloidal silica) to separate organisms from sediments. The observed animals were stained with Rose Bengal and then counted.
The first 120 nematodes from each replicate were selected, placed in glycerin and then mounted on slides for identification to species level. In case of individual number lower than 120, all the nematodes were isolated. Species name was harmonized according to NeMys online identification system (Vanaverbeke et al., 2004).
Regarding the feeding type classification proposed by Wieser (1953), all nematodes were grouped as: (1A) selective deposit feeders, (1B) non-selective deposit feeders, (2A) epistrate (diatom) feeders, and (2B) predators/omnivores. Density per feeding group (both in number and percentage) was determined for all stations.
As described by Heip et al. (1985), Index of Trophic Diversity (ITD) was calculated varying from the highest value (0.25) to the lowest one (1.0).
Maturity index (MI) was determined as the weighted average of individual colonisere-persister (c-p) values (Bongers, 1990):
$MI = \sum v\left( i \right) \cdot f\left( i \right),$
where v(i) represents c-p value of the genus i and f(i) as the frequency of that genus. As a semi quantitative value, this index indicates ecosystem conditions considering the nematode assemblage composition.
2.2 Determination of physical and chemical parameters
Environmental parameters including depth, temperature, dissolved oxygen and salinity were recorded at all sampling stations. These parameters were measured in water column by using a CTD probe (Ocean Seven 316, Italy).
Organic matter determination was performed by drying sediment samples at 70°C for 24 h and then combusting in an oven at 550°C for 4 h. As declared by Abrantes et al. (1999), total organic matter (TOM, %) was calculated by the following equation:
$TOM = {\rm{ }}\left[ {\left( {B - C} \right)/B} \right] \times 100,$
where B and C are the weights of dried sediment before and after combusting in the oven, respectively.
Sediment grain size analysis was made from sediment samples collected in separate polythene bags. For that, samples were air dried and sieved through a mechanical sieve to remove shells, debris, etc. Dried sediment samples were subjected to size fraction analysis following the procedure of Wentworth (1992). Hundred grams of sample was taken and sieved through a 62 lm mesh-sized screen for 10 min in a mechanical sieve shaker. The sample that remained in the sieve was weighed and treated as sand. The sediment samples which passed through the sieve were the mud (silt and clay).
2.3 Metals analysis
As shown in Fig. 1, sediment samples were collected from the six stations using Van-Veen grab for metal analysis. After packing in plastic bags, samples were carried to the laboratory in iced-boxes and stored at 4°C until analysis.
Sediment samples were dried in an oven, ground by using a hand mortar and then screened through a 0.5-mm mesh size sieve to remove large particles. Sediment sample digestion (0.5 g each sample) was carried out using a mixed solution of HF-HCl-HNO3-HClO4 according to the ASTM standard practice D5258-92 (ASTM, 2013).
Samples were analyzed for Al, As, Cu, Ni, Pb, Co, Cr, V and Zn by using inductively coupled plasma-optical emission spectrometry (ICP-OES; Varian VISTA-MPX). A good agreement was found between the analytical results of the quality control samples with the certified values.
2.4 Statistical analysis
Univariate indices of community parameters including density (N, ind./(15.20 cm2)), number of species (S), species diversity [Shannon diversity index, (H, log2)], species richness [Margalef’s (d)] and evenness Pielou’s (J) were calculated using statistical package of PRIMER Ver. 5 (Clarke and Warwick, 2001).
In order to evaluate the relationships between nematode community composition and environmental variables, first, a Detrended Canonical Correspondence Analysis (DCCA) was applied on non-transformed abundance data to obtain the length of gradient along the first axis according to Ter Braak and Smilauer (2002); when the gradient length is less than 3, a redundancy analysis (RDA) is recommended, while for gradient length more than 4, a canonical correspondence analysis (CCA) is suggested.
Regarding to our short length gradients in DCCA analysis, the linear model of RDA was then selected as appropriate model for the dataset. All data were lg(x+1) transformed in order to reduce the influence of common taxa. Furthermore, data were centered and standardized by species to harmonize different scales (Lepš and Šmilauer, 2003).
Monte Carlo permutation test was executed to determine whether the relation between species abundances and the measured physicochemical variables was significant. These analyses were performed using the software of CANOCO 4.5 (Ter Braak and Smilauer, 2002). The relationships amongst various biological and environmental parameters were tested by Spearman correlation analysis.
3 Results
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3.1 Environmental variables
Environmental parameters data of the studied area are presented in Table 1. The range of depth was between 6.8 m and 14.85 m with the highest and the lowest depths at Stas E and A, respectively. The average depth was (11.63±3.14) m. Concerning to the analysis, TOM content in sediment of the studied area varied from 1.92% to 7% with an average value of 3.95%±1.93%. Stations F and A exhibited the highest and the lowest TOM amounts. In addition, the average contents of sand and mud were 68.87%± 34.38% and 31.12%±34.38%, respectively (Table 1). Average concentrations of As, Co, Cr, Cu, Ni, Pb, V and Zn were (10.16±3.65) μg/g, (29.66±4.50) μg/g, (110.5±20.56) μg/g, (22.16±10.30) μg/g, (49.16±11.33) μg/g, (15.33±3.26) μg/g, (136.66±33.35) μg/g and (73±17.52) μg/g, respectively (Table 1).
3.2 Nematode assemblage
As presented in Table 2, 15 nematode species belonging to 11 genera were identified at the sampling sites. From total individuals, Xyalidae and Tripyloidoidea had dominantly the highest individuals with 66.54% and 12.95%, respectively.
Numerically, Genus Daptonema with five species was dominant. The highest and the lowest frequency at the sampling sites were dedicated to D. curticauda and H. minusculus (Table 2). As summarized in Table 3, D. curticauda, D. tenuispiculum, D. robustus were identified at all sampling sites while other species were present at some stations (Table 3). There were differences in total nematode density (N) among sampling sites. Stas D and F had the maximum and the minimum densities, respectively (Table 3). Overall mean density of nematode inhabiting in sediment of the studied area was 139.78±98.91 (ind./(15.20 cm2)). Shannon diversity index (H) ranged between 1.11 and 2.69 with average value of 2.12±0.55. The most and the least values of Shannon diversity index was recorded at Stas A and F, respectively (Table 3). Species richness (d) ranged between 0.67 and 1.58 and displayed the highest and the lowest values at Stas C and F, respectively.
As showm in Table 3, species richness averaged 1.26±0.32 and indicated differences among sampling sites (Table 3). The highest and the lowest MI value were obtained at Stas F and E, respectively. The minimum (maximum trophic diversity) and maximum (minimum trophic diversity) of ITD were measured 0.59±0.10 at Sta. F and 0.79±0.07 at Sta. C, respectively (Table 3).
Regarding the results of SIMPER analysis, genus Daptonema was the most impacted taxa at all stations as high abundances of D. curticauda, D. tenuispiculum and also T. marinus were discovered throughout the studied area (Table 4).
Percentage of each feeding type is shown in Fig 2. In most sampling sites, non-selective deposit feeders (IB) were dominant group, followed by epistrate feeders (2A).
Limited distribution of predators/omnivores (2B) was only revealed at Stas A and F while selective deposit feeders (1A) were presented at Stas A, C and E.
3.3 Relationship between nematode and environmental variables
As illustrated in Fig. 3, the first two RDA axes showed high eigenvalues (0.49 and 0.25, respectively) in comparison to subsequent axes and explained 49.3% and 25.8% of the variation in species composition, respectively. On the whole, both axes explained 75.1% of variance of species-environment relation (Fig. 3).
Furthermore, RDA analysis exhibited an association between A. araelensis with high values of As, Cu and Mud. Positive correlations were observed between abundances of A. spinosus, H. minusculus, H. brachystoma and T. flevensis with Cr, V and Co values. There was a negative correlation between sand and A. realness abundance (Fig. 3).
3.4 Relationship between environmental variables and biological parameters
According to Pearson’s analysis, a positive correlation was detected between depth and all the elements (Table 5). The whole elements, except for Cr, were positively correlated with mud. Also, all the elements had positive correlations with TOM. There were negative correlations between H, J and N with the whole elements. A negative correlation was found between diversity indices and TOM (Table 5). Significantly, positive correlations were discovered between MI with As, Cu and mud (p<0.01). Moreover, ITD was negatively correlated with mud, As, Cu and TOM (p<0.05).
4 Discussion
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Two sets of SQGs developed for marine and estuarine ecosystems (MacDonald et al., 1996; Long and MacDonald, 1998) were applied in this study to assess the ecotoxicological risk assessment of metals in sediments: (1) the effect range low (ERL)/effect range median (ERM) and (2) the threshold effect level (TEL)/probable effect level (PEL) values. Low range values (i.e., ERLs or TELs) are concentrations below which adverse effects upon sediment dwelling fauna would infrequent be expected. In contrast, the ERMs and PELs represent chemical concentrations above which adverse effects are likely to occur (Long and MacDonald, 1998). At all sampling sites, concentrations of Pb and Zn were lower than the relevant values of effects range low (ERL). A decrease in As, Cr and Cu contents were in the range between ERL and ERM, proposing that these metals would be anticipated rarely to cause adverse biological effects on biota (Long et al., 1995) in the studied areas. Furthermore, Ni levels were higher than ERM at some sampling sites, implicating that negative eco-risk effects often occur at Stas B and F. All elements, except for Cr and V, showed high positive correlations with mud, depth and TOM. The results presented here, suggested the impact of sediment grain size, depth and TOM content on metal distributions (Pb, Zn, As, Cu, Co and Ni) in the studied area. Generally, sediment grain size becomes finer as depth increases. Sandy sediments are made in coastal areas due to their much weight, and the amount of large-sized sediments decreases off shore, while fine-sized sediments increase when coming on shore. The fine grains, representing the higher rate of surface to volume and ionic absorption power, are more capable in the absorption of contaminated organic and inorganic materials (McCave, 1984; Horowitz and Elrick, 1987). Generally, fine-grained sediments carrying lots of organic matter are more contaminated than coarse-grained sediments. By contrast, the presence of a week correlation between Cr and V with sediment grain size, depth and TOM might indicate the possible effect of other parameters on their concentrations. Sediment grain size and organic matters has been proposed as dominant factors elucidating a significant part of the variance in species composition of nematode assemblages (Heip et al., 1985). Additionally, water depths seemed to be potentially important which influence the structure of nematode assemblage, probably by determining other factors like as TOM and the stability of physico-chemical factors. Both the amount of organic matter and oxygen content are also determined by the sediment grain size, as the highest oxygen penetration depth with the lowest organic matter is generally observed in coarser sediment (Castro and Huber, 2003). Several investigators have reported the increased density and diversity of marine nematodes with increased sediment grain size (Vanaverbeke et al., 2011; Fonseca et al., 2014), though contradictory result has also been published elsewhere (Maria et al., 2013), implying that their response is species-specific. In our survey, the abundance and diversity indices of nematodes were negatively affected by depth, mud and TOM while they showed a positive correlation with sand. This is probably due to the organic matter enrichment in muddy station which can decrease total density and species number of nematode by creating a hypoxia inside the sediment; thus change their community structure (Armenteros et al., 2009, 2010). But a higher density and species number is commonly observed in coarser sediments, where a deep penetration of oxygen is occurred by active flows through the sediments (de Beer et al., 2005).
Some typical effects of metals exposure and hydrocarbons contamination including changes in nematode assemblage structure, mortality of the most sensitive species and decreased diversity have been demonstrated by several authors (e.g., Boucher, 1980; Tietjen, 1980; Somerfield et al., 1994; Danovaro et al., 1995; Austen and Somerfield, 1997; Beyrem and Aissa, 2000; Mahmoudi et al., 2002; Hedfi et al., 2007, 2008; Boufahja et al., 2011). Although nematode abundance might not be affected, a great deal of studies have informed a significantly metal-induced decrease in nematode abundance.
As previously reported by Somerfield et al. (1994), there were less abundance, lower richness and species diversity of nematode fauna in copper-contaminated sites as compared to the one from less contaminated areas. Correspondingly, negative correlation was found between N, J and H with all the metal contents in this study. Metal accumulation in the sediments might change the associated microbial communities; consequently affecting the meiobenthose through changes in food supply (Austen and McEvoy, 1997). Millward and Grant (1995) documented that a certain selection for more tolerant species occurs only after longer periods of exposure to metals, which affects the community composition: the number of tolerant nematode species against Cu increased along an estuary enriched with copper in comparison to unpolluted reference sites.
Many researchers exhibited that there are adapted species with a high tolerance to metal compounds among nematodes (e.g., Molgolaimus demani, Sabatieria pulchra, Axonolaimus paraspinosus, Oncholaimus campylocercoides, Bathylaimus capacosus; Warwick, 1988; Somerfield et al., 1994; Hedfi et al., 2007). Moreover, as detected by Somerfield et al. (1994), adaptive effects may expand the tolerance range within the same species like as Enoplus brevis (Nematoda) from a contaminated site was more tolerant than specimens from uncontaminated sites. In the present study, the association between A. araelensis with high values of As, Cu and mud infer that this species can tolerate medium levels of As and Cu. As demonstrated by laboratory studies, in addition to the chemical form of a metal, other parameters including temperature (Lehtinen et al., 1984; Vranken et al., 1989), salinity (Bengtsson and Bergström, 1987) and food (Verriopoulos and Moraitou-Apostolopoulou, 1989) can influence on acute and sublethal toxicity of metals to a variety of meiofauna. Nematodes can uptake metals through the cuticle (Howell, 1983) and the secretion of mucous substances makes them capable of binding metals. Riemann and Schrage (1978) proposed mucus as a part of feeding mechanism in many nematode species. Another explanation for metals assimilation in meiofauna is metal binding capability of acid mucopolysaccharides secreted by the bacteria, as many nematodes and copepods are bacterial feeders (Jensen, 1987). According to our results, some species, such as A. spinosus, H. minusculus, H. brachystoma and T. flevensis can tolerate high range of Cr, V and Co; thus they posses some form of tolerance mechanism. Increased metals led to a decrease in abundances of A. elegans, Chromadorita sp.1, D. curticauda, D. karabugasensis, D. robustus, D. setosum, D. tenuispiculum, M. naidinae, S. cuneatus. Hence, they seemed to be intolerant species to metal. In previous study by Moreno et al. (2011), who compared the use of different ecological indices, including H, MI, c-p%, ITD and the presence of sensitive/tolerant genera at many different sites in the Mediterranean Sea, the use of nematodes has been proved as the best tool for efficient evaluation of ecological quality status.
Regarding TOM content, all sites showed a high/good EQS (Tables 6 and 7). Based on metal concentration, the majority of sites displayed a moderate EQS, except for B and F, which revealed a poor/bad EQS (Table 7). Summarizing the presented results based on these variables, it can be inferred that A, C and D were the ones described by greater environmental quality, whereas Stas B and F were characterized by lower environmental quality.
The maturity index is also used to assess the EQS at different sites, even though its utilization is arguable in marine and brackish ecosystems (Bongers et al., 1991; Neilson et al., 1996; Essink and Keidel, 1998; Mirto et al., 2002; Fraschetti et al., 2006; Gyedu-Ababio and Baird, 2006; Moreno et al., 2008a, b). Principally, the maturity index is based on various strategies of nematode assemblage in relation to different disturbances. Considering this index, Sta. F represented a high EQS whilst a poor EQS was discovered at Stas A, B, C, D and E. In order to correlate the trophic diversity of nematodes with pollution levels, the index of trophic diversity is usually used (Heip et al., 1985; Mirto et al., 2002). The application of this index revealed a poor/bad EQS at Stas A, B, C, and D while Sta. F displayed moderate EQS (Table 7). In accord with the Shannon diversity index, a poor EQS was discovered at Stas B, C, D, E and F while a moderate EQS was assigned to Sta. A (Table 7). In stressed environments subjected to organic enrichment, human disturbance and physical stressors, values of the Shannon diversity index decreased which is implicated to a reduction in biodiversity (Fraschetti et al., 2006; Bianchelli et al., 2008; Danovaro et al., 2008). ITD, H and MI indices indicated that Stas B, C, D, E have lower environmental quality. Generally, chemical and biological indices displayed different results while biological indices showed similar findings in more sites.
This study showed the differences in marine nematode communities caused by environmental parameters and indicated that the nematode communities were notably influenced by metals contamination. Because in the present work, the nematode assemblages were investigated only in autumn, more studies during other seasons, within at least two or three successive years and with increasing the sample size, are needed to fully understand how nematode respond to metals contamination and other environmental parameters. Furthermore, the use of different ecological indices showed various results; hence determination of the best indicator would be important in future studies for the evaluation of environmental quality status.
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doi: 10.1007/s13131-017-1051-x
  • Receive Date：2016-05-10
  • Online Date：2026-04-16
  • Published：2017-10-01
Article Data
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History
  • Received：2016-05-10
  • Accepted：2016-08-03
Affiliations
    1 Iranian National Institute for Oceanography and Atmospheric Science (INIOAS), Tehran 1411813389, Iran
    2 Department of Fisheries, Faculty of Animal Science and Fisheries, Sari Agricultural Sciences and Natural Resources University, Sari 578, Iran
    3 Department of Environmental Science, Faculty of Environment and Energy, Science and Research Branch, Islamic Azad University, Tehran 1477893855, Iran
    4 Department of Marine Science and Technology, Tehran North Branch, Islamic Azad University, Tehran 1477893855, Iran

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表12种不同金属材料的力学参数
科
Family		 属数
Number of
genus		 种数
Number of
species		 占总种数比例
Percentage of
total species (%)		 属
Genus		 种数
Number of
species		 占总种数比例
Percentage of total
species (%)
鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
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