Marine Biodiversity

, Volume 48, Issue 1, pp 139–151 | Cite as

Nematode communities in the Sai Gon River harbors in relation to tributyltin concentrations

  • Ngo Xuan Quang
  • Nguyen Thi My Yen
  • Nguyen Van Dong
  • Larisa Prozorova
  • Nic Smol
  • Lidia Lins
  • Ann Vanreusel
MeioExtreme
  • 105 Downloads

Abstract

The impact of toxic tributyltin (TBT) compounds was investigated on free-living nematode communities in the Sai Gon River. Samples were collected from 11 harbor stations downstream of the Sai Gon river plus one upstream station during the dry and rainy seasons. The results showed that all butyltin compound (mono-, di-, and tri) concentrations were relatively low compared to historical data from the same or adjacent estuaries, supporting the effectiveness of the 2009 ban on these products as antifouling. Nematode communities were typical for oligohaline regions showing a high spatial and temporal variability in abundance and diversity. Nematode community composition clearly differed between the two seasons, with the nematode communities being less variable in the rainy season compared to the dry season, while nematode communities differed significantly between stations. TBT values were still significantly negative correlated with nematode densities and selective deposit feeders during the dry season, partly confirming earlier experimental results on the response of nematodes to TBT. The historical presence of TBT contamination can possibly have caused a long-term impact on nematode communities in the Sai Gon river sediment, reflected in depressed densities during the dry season.

Keywords

Nematode communities Environment Pollution Butyltins Antifouling effects Seasonal effects Sai Gon river Vietnam 

Introduction

The Sai Gon River plays an important role for the economic development and water supply of more than 8 million people in Ho Chi Minh city, Vietnam (Fig. 1). However, this river is facing ecological problems due to pollution effects, such as from the antifouling compounds tributyltin (TBT) and its degradation products dibutyltin (DBT) and monobutyltin (MBT) (Sarradin et al. 1995; Dowson et al. 1996; Diez et al. 2002). Until recently, the use of TBT as an antifouling product was responsible for contaminating the water and sediments in the downstream part of the river. TBT is an extremely toxic substance belonging to the group of endocrine disrupting chemicals (EDC) which interfere with most metazoan endocrine systems and produce adverse developmental, reproductive, neurological, and immune effects (Höss and Weltje 2007). However, its use to prevent fouling by aquatic organisms on boats and to preserve constructions in harbor docks was until recently uncontrolled in Vietnam.
Fig. 1

Sampling stations in the Sai Gon river, Vietnam

Before its ban since 2009 in Vietnam, tributyltin was found frequently in the sediment in variable concentrations, up to 50 ng/g along the south coast and in the Sai Gon river (Midorikawa et al. 2004; Dang et al. 2005; Takaomi et al. 2008). The accumulation of this toxic substance in the sediment may be lethal for various aquatic organisms, including eukaryotes and prokaryotes (Alzieu et al. 1989; Ballmoos et al. 2004). At San Diego Bay, the effect of TBT on the benthic fauna resulted in significant changes in the community composition in relation to TBT concentrations in both water and sediment (Lenihan et al. 1990). These authors mentioned that TBT is among the most toxic chemicals ever introduced into the marine environment by man. It can be 100–1000 times more toxic than either copper or zinc (Short and Thrower 1986; Mayer 1987). Moreover, the effects of TBT on the meiofauna, especially on its dominant group, the nematodes, have also been studied (e.g., Austen and McEvoy 1997; Schratzberger et al. 2002; Hoshi et al. 2003; Höss and Weltje 2007). Austen and McEvoy (1997) showed by means of a laboratory experiment that nematode species richness and abundance responded negatively to different levels of TBT contamination. Some genera such as Terschellingia, Sabatieria, and Daptonema were found to be more dominant in the TBT medium treatment of Lynher estuary mud (Austen and McEvoy 1997). A study on the effect of 17-beta-estradiol, bisphenol A and tributyltin chloride on Caenorhabditis elegans by Hoshi et al. (2003) confirmed that these chemicals had a negative impact on the number of germ cells in the reproductive system of this nematode. Tominaga et al. (2002) also found significantly reduced reproduction and number of males of C. elegans.

Schratzberger et al. (2002) studied the effects of paint-derived tributyltin on the structure of estuarine nematode assemblages in experimental microcosms. They suggested that the effects of TBT are likely to occur through the uptake of leached TBT from the sediment pore water through the permeable nematode cuticle, resulting in decreased diversity and changes in assemblage structure with increasing levels of TBT contamination. In addition, the authors assumed that a direct ingestion of paint-particles with food resulted in a significant decline of non-selective deposit feeders in contaminated sediments. Moreover, their work illustrated that the response of nematode species depended not only on the level of TBT contamination but also on the duration and mode of exposure to contaminated sediments, which should be taken into account when assessing the effects of TBT on aquatic communities. In this regard, the effect of TBT and its degradation products on the benthic fauna is not only responsible for a decrease in density and diversity of more sensitive organisms but also for a negative effect on the trophic diversity, and consequently on the ecosystem functioning (Schratzberger et al. 2002).

As mentioned above, nematodes represent the most abundant group belonging to the meiofauna (<1 mm) (Giere 2009). Moreover, they are very diverse, ubiquitous, and represented by different feeding types and life strategies (Bongers 1999). In addition, nematodes also exhibit different levels of tolerance to changes in environmental conditions and to toxicant effects (Monteiro et al. 2014), which makes them ideal organisms in studies involving the effect of pollutants on the community structure and standing stocks.

In this study, we sampled the nematode communities in different harbors along the GRiver 5 years after the ban on the use of TBT. The objectives of this study were: (1) to describe the nematode communities from the Sai Gon river harbors for the first time; (2) to measure the levels of TBT concentrations and its degradation products in the sediments; and (3) to evaluate the effect of TBT concentrations on the current nematode communities as shown in previous experimental studies (Austen and McEvoy 1997; Dahllöf et al. 2001; Schratzberger et al. 2002). More specifically, we tested the hypothesis that total nematode diversity and densities, and the abundance of non-selective deposit feeders, was lowest at the highest TBT concentrations.

Methodology

Study area and sampling design

The sampling was carried out in both the dry (March) and wet (September) seasons of 2014. During both sampling campaigns, triplicated sediment samples for chemical and biological analysis were collected at 11 stations (SG2–SG12) from different harbors in addition to one site (SG1) in the Cu Chi district, about 80 km upstream and as such far from any harbor activities (Fig. 1). All 11 harbor stations were located in the most economical active part of the Sai Gon river with different port and ship building activities taking place. All stations are regularly spread and only 1–2 km separated them from each other.

Vietnam consists of two geographical parts with different climate conditions. While the northern part of the country falls in the temperate climate zone, the study area situated in the southern part has a tropical climate with only two2 seasons: wet and dry. The wet season runs from May to November and the dry season begins in December and runs until April. Even though the temperature does not fluctuate much over the whole year in the south, the climate still differs between the two seasons, especially due to the precipitation.

Environmental sampling

Sediment samples for total organic carbon and butyltin compounds (MBT, DBT- and TBTn) were analyzed in the laboratory. Other environmental variables such as pH, conductivity, salinity and oxygen redox potential (ORP) were directly measured on the overlying bottom water at the sampling locations by means of a portable tester (model YSI pH 100; Schott HandyLab, USA).

Sediment samples were collected using a Ponar-type grab and kept in glass bottles for transport to the laboratory (Department of Analytical Chemistry, Faculty of Chemistry, Ho Chi Minh City University of Science) where they were wet-sieved through a 0.063-mm sieve using filtered water collected from the same locations. After centrifuging and decanting, the sieved fraction was collected and kept frozen for analysis of butyltin and total organic carbon. The residual was removed because organotin desorption from sediment does not occur during the wet-sieving with overlaying water (Quevauviller and Donard 1991). Unfortunately, residues were not kept for the originally planned granulometric analysis.

Environmental sediment treatment and analysis

MBT (95%), DBT (96%), TBT (96%), and tripropyl tin (TPrT) (98%) as chlorides were purchased from Aldrich, Germany, and deuterated tributyl (d27-TBT) was obtained from Hayashi Pure Chemical Industries (Osaka, Japan). Sulfuric acid (H2SO4, 98%, p.a. grade), hydrobromic acid (HBr, 47%, p.a. grade), methanol (MeOH, HPLC grade), dichloromethane (DCM), hexane, octane, tetrahydrofuran (THF, p.a. grade), glacial acetic acid (p.a. grade), sodium acetate trihydrate (p.a. grade), potassium iodide (KI, p.a. grade), silver sulfate (Ag2SO4, p.a. grade), magnesium perchlorate (Mg(ClO4)2, p.a. grade) and potassium dichromate (K2Cr2O7, p.a. grade) were purchased from Merck. Tropolone (98%) was obtained from Sigma Aldrich (Germany). Sodium tetraethylborate, NaBEt4 (98%), was obtained in a sealed septum vial from Galab, Geesthacht, Germany. All the OT stock solutions (1000 μg g−1 as tin) were prepared in MeOH and stored at −20 °C in 20- or 40-ml glass vials provided with silicon/Teflon septum caps (Vertical Chromatography) until use. The solution used for derivatisation was prepared by injecting 20 ml of THF into the vial containing 5 g NaBEt4 and was stored at 20 °C. A pH 5 buffer (2 M), prepared from glacial acetic acid (Merck, p.a. grade) and sodium acetate (Merck, p.a. grade), was used.

Butyltin analysis

Samples of 5 g or 0.5 g of BCR-646 were weighed in a 40-ml threaded glass bottles, provided with silicon/Teflon septum caps. The samples were wetted with MeOH and gravimetrically spiked with 100 μl d27-TBT (2.0000 ng/g as Sn in MeOH) and 100 μl TPrT (2.0000 ng/g as Sn in MeOH) then equilibrated overnight (4 °C).

The spiked samples, after addition of 10 ml HBr 2 M, were exposed to ultrasonic agitation for 15 min. After cooling and addition of 20 ml tropolone (0.04%) in DCM, the samples were shaken for 1 h and centrifuged for 15 min at 1200 rpm. The organic phase was transferred to a new glass vial and vented under argon. The residues contained in 10-ml thread tube with Teflon-lined cap were re-dissolved in 1 ml hexane for derivatization. Then, 50 μl of NaBEt4 25% in THF was added to the sample for derivatization. The tubes were then vortexed for 1 h and centrifuged for 15 min at 5700 rpm. The hexane phase was transferred into a SPE cartridge packed with silica gel. The ethylated butyltin compounds were eluted with 8 ml hexane:n-octane (9:1) (2 ml/min) into a 10-ml glass tube, then the solvent was evaporated with argon or nitrogen until 1 ml was left which was then transferred to a 1.5-ml GC vial. The sample was stored at −20 °C until analysis by GC-MS.

For calibration of standard solutions, the derivatization was performed in acetic/acetate buffer solution, pH 4.8. Suitable amounts of butyltin compounds in MeOH were taken into 10-ml threaded test tubes provided with Teflon-lined caps. Next, 100 μl d27-TBT (2.0000 ng/g as Sn in MeOH) and 100 μl TPrT (2.0000 ng/g as Sn in MeOH) were gravimetrically spiked followed by 1 ml bi-distilled water and 1 ml acetic/acetate buffer solution (pH 4.8,1 M), followed by 50 μL of NaBEt4 25% in THF added for derivatization. The tubes were then vortexed for 1 h and centrifuged for 15 min at 5700 rpm. The hexane phase was transferred into a 1.5-ml GC vial and stored at −20 °C until GC/MS analysis for butyltin species.

A 7-point calibration curve for the quantitation of MBT, DBT and TBT was made from a mixed MBT, DBT and TBT interim standard solution containing 10 ng/g as Sn in MeOH for each compound. TPrT was used as internal standard for the quantitation of MBT and DBT. D27-TBT, was used as internal standard for quantitation of TBT.

The separation of alkylated butyltin species were performed by GC (Trace GC, 2000 series; Thermoquest, USA) using a DB-5 capillary column (length 30 m, i.d. 0.25 mm, film thickness 0.5 μm) and the detection/quantitation was carried out using MS (Automassmulti; Thermoquest).

The isotope dilution analysis (IDA) was used to calculate the TBT concentrations to provide highly reliable data since all possible losses or species transformation are corrected. For MBT and DBT, the quantitation is based on calibration using TPrT as IS to correct for variations in sample preparation and injection to GC. The analytical method for butyltin speciation was demonstrated to be free from species transformation. All concentrations are given on a dry weight basis as Sn. The accuracy of the analytical procedure was also evaluated using CRM BCR-646.

Total organic carbon analysis

The total organic carbon (TOC) was determined by wet combustion as described by Nelson and Sommers (1982). Briefly, the sediment sample was digested in a mixture of H2SO4:H3PO4 (6:4) containing K2Cr2O7. The evolved gases were passed through a purifying train including 5 traps, the first containing KI and the second containing Ag2SO4 to remove Cl2, the third trap containing concentrated H2SO4 to remove water, the fourth trap containing granular Zn to absorb acid fumes, and the last trap containing Mg(ClO4)2 to absorb water. After the purifying train, the evolved CO2 was passed through a pre-weighted trap containing a 3-cm layer of granular NaOH. After the wet combustion was completed, the CO2-absorbed trap wasis weighed and the amount of CO2 calculated by the gain in the weight of the trap. The system was calibrated using potassium hydrogen phthalate. The blank measurement was carried out in identical conditions using quartz sand as the blank sample.
$$ \mathrm{Calculation}: TOC\ \left(\%\right)=\frac{m_{CO_2(sample)}-{m}_{CO_2(blank)}}{m_{dried\ sample}}\times 0.2727\times 100 $$

Biological sample collection and nematode identification

In each station, 5- to 10-m-deep triplicated sediment samples were collected using a ponar grab. Only samples with clear overlying water and with sediment up to 10 cm depth were retained. Sediment from the grab was subsampled by means of a transparent core of 3.5 cm diameter. Samples were preserved in 70 °C formaldehyde at 7%. Nematodes were extracted from the sediment by sieving through a 1-mm sieve and keeping the fraction retained on a 38-μm sieve. Then, the meiofauna was separated by the flotation technique using Ludox-TM50 (specific gravity 1.18) (Vincx 1996). In order to facilitate sorting of the nematodes, the samples were stained with 1% solution of Rose Bengal. All nematodes in the samples were counted under a stereomicroscope. About 200 nematode specimens were picked out randomly per sample and processed into permanent slides following De Grisse (1969).

All selected nematodes were identified up to genus level by using the pictorial key on Free living Marine Nematodes, Part III (Warwick et al. 1998), the Identification manual for freshwater nematode genera (Zullini 2005, and unpublished; Bongers 1988; Nguyen 2007), together with other articles and the NEMYS database (Guilini et al. 2016).

Data analysis

Data of nematode communities

The Shannon diversity index (H′) (Shannon 1948) was calculated based on the proportional abundances pi of each genus [abundance of the species (Ni) per total abundances (Nt)]:H′ = −Σ [pi × log (pi)], in which pi = Ni/Nt = relative abundance of the ith genus. The univariate data (Shannon diversity index, genus richness, and proportion of non-selective deposit feeders) were tested for significant differences based on resemblance matrices derived from Euclidean distances using the software PRIMER v.6 (Anderson et al. 2008). A non-parametric permutational ANOVA (PERMANOVA) was conducted using a two fixed-factor crossed design comprising ‘station’ and ‘season’ as factors. Significant values were considered when p < 0.05. After the PERMANOVA routines, pairwise pseudo t tests were executed to identify which pairs of stations were significantly different from each other. Subsequently, PERMDISP routines were performed to test for homogeneity of multivariate dispersions, indicating location differences through equally dispersed distance to centroids.

Multivariate statistics based on the nematode community structure (standardized to sample totals) were performed using a Bray–Curtis resemblance matrix. The same two-factor design was used as described for the univariate community data followed by the PERMDISP analysis. Following the PERMANOVA analysis, SIMPER analysis was performed based on the nematode community relative abundance. SIMPER routines allow the identification of the taxa responsible for similarities and dissimilarities between stations and seasons as well as the contribution of each taxon to the average Bray–Curtis dissimilarity between groups of samples. The SIMPROF technique was used to test for significant differences between station groups. MDS plots (non-metric multi-dimensional scaling analysis) were used to produce 2D graphs in order to visualize the similarity patterns (Clarke and Warwick 2001).

Data analysis of environmental variables

Significant differences between stations and seasons for environmental variables were also tested by two-way non-parametric PERMANOVA. The multivariate environmental data (pH, salinity, ORP, TOC, MBT, DBT, and TBT) matrix was first normalized andthen a resemblance matrix was built based on Euclidean distances. Subsequently, correlations between environmental variables were analyzed using Draftsman plots. DistLM (distance-based linear model) analyses were conducted for environmental variables with correlations lower than 0.9. This analysis was performed to identify which environmental factors were significantly responsible for the variability observed at the nematode multivariate community structure The DistLM model was performed using a step-wise selection procedure and adjusted R 2 as selection criteria. Results from the DistLM could be visualized using dbRDA (distance-based redundancy analysis) plots.

Non-parametric Spearman rank correlation coefficients were computed (p < 0.05) to identify correlations between environmental variables and univariate indices of the nematode assemblages. Correlation tests were processed by the software STATISTICA 7.0.

Mean values are always shown in association with standard deviations.

Results

Characterization of the environment

The environmental characteristics of the overlying water (pH, conductivity, salinity) and of the sediment (oxygen redox potential and total organic carbon) for the 12 sampled stations of the Sai Gon River are shown in Table 1. The results indicated that especially salinity and conductivity fluctuated between both sampling events. During the wet season, a larger volume of fresh water runs off from the sources downstream which is reflected in low salinity values (PSU of 0) in all stations. Contrastingly, in the dry season, marine water flows until 80 km upstream, resulting in slightly elevated salinity values (2.3–3.4 PSU) except at SG1. The pH was highest at SG10 during the wet season (8.92), while in general showing lower levels (5.8–6.93) during the dry season in all stations compared with the wet season (6.8–7.95). Sediment oxygen redox potential was always negative, indicating that the sediment was mainly anoxic for all sampled stations. TOC showed no consistent patterns either between seasons or along the river, exhibiting values between 13.7 and 106.5 mg/g.
Table 1

Environmental variables measured at Sai Gon River stations (St.) during the dry (D) and the wet season (W)

St.

pH

Conductivity (μS/cm)

Salinity (PSU)

ORP (mV)

TOC (mg/g)

D

W

D

W

D

W

D

W

D

W

SG1

5.80

7.34

79

140.1

0.00

0

−280

−120

32.2

17.3

SG2

6.58

7.52

4490

144.0

2.30

0

−81

−95

21.7

19.5

SG3

6.70

7.61

4570

150.3

2.40

0

−102

−123

30.5

106.5

SG4

6.66

7.08

4690

145.4

2.50

0

−154

−150

29.1

20.7

SG5

6.68

7.95

5050

132.5

2.70

0

−164

−146

24.3

19.4

SG6

6.68

7.13

5190

124.6

2.70

0

−143

−252

29.1

15.8

SG7

6.68

7.34

5210

158.0

2.80

0

−146

−290

24.1

15.6

SG8

6.75

7.07

5155

102.7

2.90

0

−157

−339

22.5

35.5

SG9

6.81

6.81

5155

156.0

2.6–2.9

0

−170

−275

20.3

28.9

SG10

6.82

8.92

5090

103.9

2.70

0

−191

−307

23.5

22.9

SG11

6.81

6.85

4920

88.9

2.60

0

−192

−398

20.3

13.7

SG12

6.93

7.15

6210

51.6

3.40

0

−196

−345

18.8

39.4

The pH, conductivity, and salinity values were measured for the overlying water, while oxygen redox potential (ORP) and total organic carbon (TOC) were measured for the sediment

Butyltin compounds showed high variation both between the sampling stations and seasons (Fig. 2). MBT ranged from 0.37 ± 0.11 to 6.08 ± 0.22 ng/g in the dry season and from 0.08 ± 0.14 to 4.02 ± 0.18 ng/g in the wet season. The two-way PERMANOVA results indicated that MBT values were significantly different between seasons (p se = 0.001), stations (p st = 0.001) while it also showed a significant interaction between the two terms (p se&st = 0.001). DBT concentrations varied between 0.09 ± 0.06 and 4.62 ± 1.23 ng/g for all stations and for both seasons, and its values were also significantly different between stations (p st = 0.001), seasons (p se = 0.001) and between the interaction (p st&se = 0.001). TBT concentrations in the sediment were in general lower than the concentrations observed for MBT and DBT, with values ranging from 0.12 ± 0.11 to 4.3 ± 1.87 ng/g in the dry season and from under detection levels to 2.03 ± 1.23 ng/g in the rainy season. TBT concentrations could not be detected in SG10 and SG11. Significant differences in TBT concentrations were found between stations (p st = 0.0002) and for the interaction between season and station (p se&st = 0.0016). The pairwise comparison (supplementary material) illustrate that there is a high variability in BT compounds, especially between stations. Station SG3 mainly showed consistently high values for all BT compounds whereas SG10, SG11 and SG12 has consistent low values.
Fig. 2

Average and standard deviation of a monobutyltin (MBT), b dibutyltin (DBT) and c tributyltin (TBT) concentrations in the dry season (D) and wet season (W) in the Sai Gon River

Nematode communities in the Sai Gon River

The densities of nematodes showed a high spatial and temporal variability across stations and between seasons. Densities ranged from 13.3 ± 2.9 ind./10 cm2 to 408.7 ± 142.5 ind./10 cm2 in the dry season and from 58 ± 41.9 ind./10 cm2 to 1649.7 ± 1462 ind./10 cm2 in the wet season (Fig. 3). The highest abundance of nematodes occurred in station SG9, followed by the stations SG1 and SG8 and higher densities were observed on average in the wet season when compared with the dry season. PERMANOVA results based on the total nematode density showed significant differences between stations and seasons (p se = 0.008, p st = 0.001) as well as a significant interaction effect (p se&st = 0.001). Pairwise comparisons (supplementary material) showed seasonal differences for the stations SG1, SG4, SG7, SG9 and SG11.. This also confirms the significant higher densities at stations SG1, SG8, SG9 and SG10 compared with most of the other stations.
Fig. 3

Densities of nematode communities in the Sai Gon River (D dry season and W wet season)

The nematode community composition of the Sai Gon River harbors consisted of species belonging to both classes, Enoplea and Chromadorea. In the dry season, species were distributed over 10 orders, 42 families and 88 genera, while for the wet season 10 orders, 45 families and 102 genera were observed.

The number of genera per station ranged from 11 to 39 in the dry season and from 21 to 37 in the wet season. Their average and standard deviation (Fig. 4a) were lowest in SG4 represented by 5 ± 1 genera, and highest in SG6 with 21.3 ± 3.8 genera. The two-way PERMANOVA analysis based on the nematode genus composition showed significant differences between seasons (p se = 0.03) and stations (p st = 0.0012) as well as between the interaction factors (p se&st = 0.0003). Pairwise comparisons showed a seasonal effect for the stations SG4 (p = 0.008), SG7 (p = 0.009), SG9 (p = 0.038), and SG12 (p = 0.005). Differences between stations were most prominent in the dry season.
Fig. 4

Average ± standard deviation of genera richness (S) (a) and Shannon index (H′) (b) of nematode communities in dry season (D) and wet season (W)

Shannon diversity showed both the lowest and the highest values in the dry season (SG7, 0.62 ± 0.67 and SG2, 3.43 ± 0.17, respectively) (Fig. 4b). Shannon values showed high spatial and temporal variability across stations and between seasons. The two-way PERMANOVA analysis showed no significant differences between seasons (p se = 0.126). Nevertheless, significant differences were observed between stations (p st = 0.001) and for the interaction terms (p se&st = 0.001). There were seasonal differences for stations SG7, SG9 and SG10, whereas similar as for stations mainly differed in the dry season from each other.

The trophic structure of the nematode communities in the dry season consisted of a high percentage of non-selective deposit feeders 1B (from 15.4 ± 13.6% to 94.2 ± 1.3%). The highest proportions of this group were found at SG7 and SG8. Epistratum feeders and predator-omnivores feeders contributed less (2A: 0.46 ± 0.79%–52.7 ± 5.7%; 2B: 1.3 ± 1.4%–36.4 ± 3.8%). There was a very low percentage of selective deposit feeders found in all stations, except for SG11 (69.4 ± 26.3%).

In the wet season, the trophic structure consisted of a high percentage of non-deposit feeders 1B (from 22.4 ± 5.85% to 89.7 ± 2.08%) in all stations. All other feeding types showed a lower percentage (1A: 1.15 ± 1.99%–40.4 ± 11.9%; 2A: 0.32 ± 0.28%–34.2 ± 8.77%; 2B: 3.02 ± 2.1%–43.1 ± 12.6%).

Multivariate analysis

The SIMPROF and MDS plot showed that the nematode communities were more different between stations in the dry season (five groups), while in the wet season all stations were grouped together except for station SG1 (Fig. 5a, b). This station was located in the upstream part and it was dominated in the dry season by genus Ironus (up to 46.6%), followed by Terschellingia (20.4%), Aphanonchus (12.9%), and Paraplectonema (10.2%). Group 2 (stations SG2, SG3, SG5) was characterized by the dominance of the genera Sphaerolaimus, Daptonema and Parodontophora. In group 3 (stations SG6, SG7 and SG8), Daptonema was dominant (69.7–96.4%). Group 4 (SG9, SG10, SG11 and SG12) was characterized by a high contribution of Terschellingia, Monhystera and Parodontophora (23.4–38.7%). In group 5 (station SG4), the genera Aphanonchus, Mylonchulus , Rhabdolaimus, Sphaerotheristus were equally abundant, with percentages varying between 23.9 and 28.4%.
Fig. 5

a MDS based on nematode genera composition of triplicate samples of stations (SG1–SG12) in the dry season. b MDS based on nematode genera composition of triplicate samples of stations (SG1–SG12) in the wet season

During the wet season, nematode communities were more clustered together, and all stations were characterized by high abundances (from 6.7 up to 84.8%) of the genera Theristus, Parodontophora, Rhabdolaimus, Terschellingia, Monhystera, Dorylaimus, Eumonhystera, Ironus, Aphanonchus, Mesodorylaimus and Paraplectonema.

Interaction between nematode communities and environmental variables, including the tributyltin compounds

Correlations between nematode univariate data (total densities, genus richness, Shannon diversity, and percentage of the four trophic groups) and environmental variables (pH, salinity, ORP, TOC, MBT, DBT, and TBT) are shown in Tables 2 and 3 for the dry and wet season, respectively. Nematode densities were significantly negative correlated with TBT in the dry season. Predators and omnivores had a positive correlation with MBT and DBT in both seasons, whereas the selective deposit feeders showed a negative correlation with MBT, DBT and TBT in the dry season. The non-selective deposit feeders were negative correlated with DBT in the wet season.
Table 2

Correlations between nematode and environmental variables in the dry season

Variables used

Correlation coeff.

pH

Conduct

Salinity

ORP

TOC

MBT

DBT

TBT

S

R

−0.101

−0.078

−0.115

−0.179

−0.004

−0.005

0.063

−0.161

p

0.559

0.653

0.505

0.294

0.980

0.975

0.716

0.349

N

R

−0.257

−0.289

−0.272

0.200

−0.078

−0.282

−0.242

−0.377

p

0.130

0.087

0.109

0.241

0.652

0.096

0.154

0.024

H′

R

−0.139

−0.12

−0.173

−0.212

0.168

0.071

0.142

0.075

p

0.420

0.485

0.314

0.214

0.328

0.682

0.409

0.664

%1A

R

−0.068

−0.284

−0.244

0.6340

−0.394

−0.476

−0.44

−0.395

p

0.692

0.093

0.152

0.000

0.017

0.003

0.007

0.017

%1B

R

0.156

0.232

0.255

−0.344

0.076

0.183

0.202

0.284

p

0.364

0.173

0.133

0.040

0.659

0.286

0.237

0.094

%2A

R

−0.632

−0.547

−0.602

0.088

0.704

−0.176

−0.175

−0.027

p

0.000

0.001

0.000

0.609

0.000

0.304

0.307

0.875

%2B

R

0.481

0.509

0.472

−0.414

−0.235

0.442

0.424

0.164

p

0.003

0.002

0.004

0.012

0.168

0.007

0.010

0.341

Environmental variables used were: pH, Conduct conductivity (μS/cm), salinity (PSU), ORP oxygen redox potential (mV), TOC total organic carbon, MBT monobultyltin, DBT dibultyltin, and TBT tribultyltin. Nematode univariate variables used: S total number of genera, N total densities, H′ Shannon diversity, and percentage of each trophic group (%1A, %1B, %2A, and %2B).

Significant results (p < 0.05) in bold

Table 3

Correlations between nematode and environmental variables in the wet season

Variables used

Correlation coeff.

pH

Conduct

ORP

TOC

MBT

DBT

TBT

S

R

0.032

−0.041

−0.055

0.088

0.098

0.063

0.065

p

0.855

0.814

0.751

0.611

0.568

0.712

0.706

N

R

−0.18

0.081

0.178

−0.062

0.108

0.007

0.075

p

0.293

0.639

0.298

0.72

0.530

0.966

0.663

H′

R

0.205

0.164

−0.395

0.025

0.161

0.239

0.146

p

0.230

0.339

0.017

0.884

0.348

0.160

0.395

%1A

R

−0.05

0.202

−0.353

−0.201

0.006

0.042

0.025

p

0.77

0.238

0.035

0.241

0.971

0.809

0.885

%1B

R

−0.124

−0.465

0.759

0.057

−0.265

−0.492

−0.277

p

0.472

0.004

0.000

0.739

0.119

0.002

0.102

%2A

R

−0.019

0.089

−0.466

0.057

0.007

0.181

0.181

p

0.911

0.602

0.004

0.740

0.968

0.291

0.290

%2B

R

0.236

0.454

−0.494

0.036

0.378

0.557

0.256

p

0.166

0.005

0.002

0.832

0.023

0.000

0.131

Environmental variables used were: pH, Conduct conductivity (μS/cm), salinity (PSU), ORP oxygen redox potential (mV), TOC total organic carbon, MBT monobultyltin, DBT dibultyltin, and TBT tribultyltin. Nematode univariate variables used: S total number of genera, N total densities, H′  Shannon diversity, and percentage of each trophic group (%1A, %1B, %2A, and %2B).

Significant results (p < 0.05) in bold

DISTLM displayed a significant effect of DBT (p = 0.001) and salinity (p = 0.0001), in explaining the variation in the nematode community composition based on the relative abundances. In addition to salinity and DBT, pH and ORP also explained the differences between stations for the dry season (p pH = 0.0001, p ORP = 0.0001). The dbRDA graph (Fig. 6) illustrates the subdivision according to season of all stations with salinity being the main driving variable responsible for the differences between seasons. Axis 1 explains 19.9% of the variation and axis 2 explains 8.8% of the variation. This plot also confirms that SG1 was the only station not showing a seasonal difference, since wet and dry seasons clustered together for this station.
Fig. 6

The dbRDA plot for both dry and wet seasons. Salinity was the main factor responsible for the significant differences found between wet and dry seasons (18 stations SG1–SG8)

Discussion

TBT concentration in the Sai Gon River in comparison with historical data from the same or adjacent estuaries

The concentrations of the antifouling product TBT and its degradation products MBT and DBT were relatively low in all harbor stations (SG2–SG12) from the Sai Gon River. In several stations (SG4–SG9), concentrations were even similar to the concentrations observed at station SG1. At this site, almost no shipping activity occurred, although other sources of butyltin may exist there, such as derived from plastics or pesticides (Díez and Bayona 2009; Chen et al. 2010). Furthermore, the tributyltin concentrations reported in our study were lower than those reported by Dang et al. (2005) from the Bason shipyard in Ho Chi Minh city, also located on the Sai Gon River, which showed TBT concentrations of 8.25–50.5 ng/g. Additionally, our values were much lower than the highest values recorded from a coastal study in south Vietnam with TBT sediment concentrations of 0.5–47 ng/g (Midorikawa et al. 2004). In general, the concentrations of butyltin in the Sai Gon River sediment measured in our study (<0.1–10.2 ng/g tin) were also low when compared with the reported values in sediment samples collected in fresh and brackish water from neighboring countries, such as China (22.95–195.60 ng/g) (Jun-Min et al. 2015), Thailand (<1–108.11 ng/g) (Nichaya and Gullaya 2014), Indonesia (50–430 ng/g) (Hiroya et al. 2013), and Taiwan (3.9–158.5 ng/g) (Cheng-Di et al. 2015), as well as from other countries (Filipkowska et al. 2014, Okoro et al. 2013). According to Dowson et al. (1993), the pollution of TBT in the sediment can be categorized in 5 levels: uncontaminated (<1 ng Sn/g), slightly contaminated (1–8 ng Sn/g), moderately contaminated (8–41 ng Sn/g), highly contaminated (41–205 ng Sn/g), and grossly contaminated (>205 ng Sn/g). According to this classification, sediment samples in the Sai Gon river were only slightly contaminated with TBT. Moreover, TBT concentrations generally decrease with time and TBT could not even be detected at some stations. These observations suggest that the imposed ban on the use of TBT was indeed effective in lowering the concentrations of this toxic pollutant in the Sai Gon River.

The main source of TBT generally comes from antifouling paints and pesticides, while significant quantities of DBT and MBT can also come from industrial activities such as chemical catalysts and additives in PVC plastics (Hoch 2001), in addition to the degradation of TBT through a sequential de-alkylation process (Rudel 2003). Most of the stations (SG2–SG12) sampled in this study were located in one of the many Sai Gon harbors, each with busy shipping traffic, and close to Ho Chi Minh, a megacity of about 10 × 106 inhabitants and surrounded by the largest industrial zones of Vietnam. The presence of butyltin compounds in this area is therefore likely to be due to the paints used on large vessels, and to the discharge of municipal wastewater.

To test to what extent TBT has disappeared from the environment as a consequence of the ban of its use as antifouling, TBT degradation was estimated using the method proposed by Díez et al. (2002). According to this method, the ratio of (TBT/MBT + DBT), known as the BT degradation index (BDI), can be used to estimate the time at which pollution had occurred. The calculated (TBT/MBT + DBT) values (Table 4) show that recent pollution by TBT of the sediments of the sampling sites is unlikely, which supports the effectiveness of the ban for almost 6 years. This time period is indeed much longer than the half-lives of TBT in sediments which amount to 360 days in freshwater sediments and 374 days in brackish water sediments (Dowson et al. 1996). Therefore, the presence of BT compounds at the sampling site (SG1) upstream of the harbor area probably originated from the tidal movement of the sediment and the discharges of municipal wastewater. The fact that the concentrations of MBT and DBT were much higher than TBT revealed that the source of MBT and DBT in these sediments were probably due to the direct discharge of BTs into the river.
Table 4

Degradation ratio of tributyltin in sediment samples

Stations

SG1

SG2

SG3

SG4

SG5

SG6

SG7

SG8

SG9

SG10

SG11

SG12

D

0.0

0.0

0.0

0.21

0.0

0.19

0.0

0.0

0.12

0.0

0.0

0.12

R

0.13

0.46

0.16

0.0

0.0

0.0

0.0

0.0

0.18

0.0

0.0

0.0

Nematode communities in the Sai Gon river harbors

Nematode communities observed in the Sai Gon river harbors were in general the typical communities normally found in oligohaline parts of estuaries inhabiting subtidal soft sediments (Ngo et al. 2016). In this regard, they showed high abundances of several freshwater nematode genera such as Dorylaimus, Aphanonchus, Rhabdolaimus, Punctodora, Eumonhystera, Paraplectonema, Ironus and Monhystera. The overall number of genera is higher in the wet season than in the dry season, but the composition of the nematode communities in the wet season was less variable between stations than in the dry season.

In addition to the high abundances of these freshwater genera, the nematode communities were also composed by the genera Terschellingia, Daptonema, Sabatieria, Theristus, Eumonhystera, Paraplectonema, Parodontophora and Thalassomonhystera, typically found in organically enriched, suboxic marine and brackish habitats (Bongers 1990, 1999; Soetaert et al. 1995).

The nematode communities from the Sai Gon river showed a high spatial and temporal variability in densities and diversity. In general, densities in this study were rather low (13–1650 ind./10 cm2) in comparison with communities from other estuarine areas (Soetaert et al. 1994; Smol et al. 1994; Moreno et al. 2008; Yodnarasri et al. 2006; Ferrero et al. 2008). Densities ranged from 168.7 to 1602.6 ind./10 cm2 at Genoa-Voltri, Portosole, and Marina degli Aregai harbors in Italy (Moreno et al. 2008); they varied between 67 and 1666 ind./10 cm2 in the Dutch Westerschelde estuary (Soetaert et al. 1994); and from 317 to 1002 ind./10 cm2 in the Shin River, the Kasuga River and the Tsumeta River in Takamatsu, Japan (Yodnarasri et al. 2006). Furthermore, our results also fall in the lower range of the subtidal nematode densities observed in the Thames river (UK), which varied between 15 and 5856 ind./10 cm2 (Ferrero et al. 2008), and in the Dutch Oosterschelde, with 100–7100 ind./ 10 cm2 (Smol et al. 1994). and at five other European estuaries with densities of 130–14,500 ind./10 cm2 (Soetaert et al. 1995).

Even though nematode communities in the Sai Gon river were characterized by a high number of genera in total over all study sites, the biodiversity values for some stations were quite low (H′ ranged from 0.62 ± 0.67 to 3.43 ± 0.17 in both dry and wet seasons) in comparison with other estuarine areas worldwide. For instance, H′ values between 1.82 and 2.37 were found in the Genoa-Voltri, Portosole, and Marina degli Aregai harbors in Italy (Moreno et al. 2008). H′ values ranged between 1.37 ± 0.75 and 2.84 ± 1.03 in the rivers Elbe (five sites), Oder (two sites), and Rhine (one site) in Germany (Heininger et al. 2007) and H′ amounted to between 0.7 and 4.71 in other German rivers (Höss et al. 2011). Similar to our results, Moreno et al. (2011) indicated a moderate H′ in harbor sites, probably because of the unfavorable conditions persisting over a long time, enabling the nematodes to adapt. However, most of the harbors considered in previous studies were only marine, while in the Sai Gon river mainly oligohaline and fresh environments can be found depending on the season investigated. In this regard, the general lower diversity and densities observed at the Sai Gon river were probably derived from its freshwater properties in the wet season, since these environments are considered to exhibit lower diversity when compared with marine environments.

Do the TBT concentrations affect the current nematode communities as shown in previous experimental studies?

In an experimental study, Schratzberger et al. (2002) found that, in the treatment with the highest TBT concentrations (at 10 ng/g), a negative effect was observed on the nematode densities. Moreover, they also found a reduction in diversity and in the abundance of non-selective deposit-feeding nematodes when the sediments were treated with TBT.

Our study also indicated a significant negative correlation between nematode densities and TBT concentrations in the dry season; however, butyltin compounds seem not to have an effect on the biodiversity of nematodes. Furthermore, the selective deposit feeders were found instead to be negatively correlated with TBT and only in the dry season. In general, the concentrations present in the Sai Gon river were much lower (TBT <3 ng/g) than the concentrations used in the experiment performed by Schratzberger et al. (2002). This may explain the weak effects only observed for nematode densities in the dry season. However, according to Schratzberger et al. (2002), the response of nematode species depends not only on the level of TBT contamination but also on the duration and mode of exposure to contaminated sediments. The historical presence of TBT contamination can possibly have caused a long-term impact on nematode communities in the Sai Gon river sediment, weakly reflected in depressed densities of the selective deposit feeders during the dry season. Possibly, the selective deposit feeders feed on particles associated with higher BT compounds, or their smaller body size results in a higher uptake through their permeable cuticle (Schratzberger et al. 2002). This needs to be explored through experimental tests on uptake mechanisms to provide further evidence.

In addition, the structure of the present nematode communities seems not only influenced by the present TBT contaminations but also by changes in other environmental factors. Especially, changes in the nematode communities between seasons were related to differences in salinity. The general low ORP present across stations also points to stressed conditions, which can result in the relatively low densities and diversity observed here when compared with other estuaries worldwide (Soetaert et al. 1994; Smol et al. 1994; Moreno et al. 2008; Yodnarasri et al. 2006; Ferrero et al. 2008). It is expected that differences in grain size also have an effect on nematode communities (Giere 2009), which unfortunately could not be tested in this study. However, assuming that differences in grain size were small, as observed during sampling, we expect that any strong negative impact of TBT would have overruled granulometric influences.

Conclusion

This study showed that TBT compounds are still found in the sediments of the Sai Gon River harbors despite the ban for more than 6 years; however, the concentrations of this compound and its degradation products were relatively low. The presence of this compound, even in low concentrations, showed negative correlations with nematode densities, especially those of the selective deposit feeders, indicating a potential negative effect of the TBT. Nevertheless, nematode communities from the Sai Gon river seemed to be mostly shaped by other environmental factors, such as salinity and oxygen conditions, which were associated with a general decrease in densities and diversity and a dominance of non-selective deposit feeders.

Notes

Acknowledgements

This research is funded by Vietnam National Foundation for Science and Technology Development (NAFOSTED) under grant number 106-NN.06-2013.66.

Supplementary material

12526_2017_718_MOESM1_ESM.docx (75 kb)
ESM 1 (DOCX 75 kb)

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Copyright information

© Senckenberg Gesellschaft für Naturforschung and Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Department of Environmental Management and Technology, Institute of Tropical BiologyVietnam Academy of Science and TechnologyHo Chi Minh CityVietnam
  2. 2.Faculty of Chemistry, Hochiminh City University of ScienceVietnam National UniversityHo Chi Minh CityVietnam
  3. 3.Federal Scientific Center of the East Asia Terrestrial Biodiversity (FSCEATB), Far Eastern Branch of Russian Academy of Sciences (FEB RAS)VladivostokRussia
  4. 4.Biology DepartmentGhent UniversityGhentBelgium
  5. 5.Marine Biology Research Group, Biology DepartmentGhent UniversityGhentBelgium

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