Veronica Borghiand and Cinta Porte Environmental Chemistry Department, IIQAB-CSIC C/Jordi Girona, 18, 08034 Barcelona, Spain Corresponding author phone: 34 93 4006175; fax: 34 93 204- 5904; e-mail: cpvqam@cid.csic.es
Aquatic pollution resulting from extensive usage of organotin compounds has been of great concern due to their deleterious effects in nontarget organisms. However, organotin contamination in deep-sea ecosystems has been rarely studied. The present work attempted to determine butyltin and phenyltin compounds in deep-sea fish collected between 1000 and 1800 m depth in the NW Mediterranean. The concentration of tributyltin (TBT) and its degradation products, mono- (MBT) and dibutyltin (DBT), as well as triphenyltin (TPT), and mono- and diphenyltin (MPT, DPT) was determined in different tissues (liver, gills, digestive tube, and muscle) of several fish species. Total butyltin residues were up to 175 ng/g wet wt, and they were comparable to levels found in coastal fish collected along the Catalan coast. In contrast, deep-sea fish contained much higher levels of phenyltins (up to 1700 ng/g wet wt), and particularly TPT (up to 1430 ng/g wet wt), than previously reported concentrations in shallow-water organisms. The obtained results confirm the long-range transport of organotin compounds to the deep-sea environment, and the subsequent exposure of fish inhabiting nonpoint source areas. The use of TPT in agriculture or as an antifouling agent, its transport to the deep-sea environment associated to particulate matter, and its nonbiodegradable nature in the food chain may account for the high residue levels detected in deep-sea organisms.
Introduction
Deep-sea regions (depth>1000 m) are poorly studied areas, that encompass about 75% of the biosphere, and are characterized by the absence of light, elevated pressures, and low temperatures. Research has demonstrated the occurrence of organochlorinated compounds, polycyclic aromatic hydrocarbons (PAHs), and heavy metals in deep-sea sediments and their uptake and bioaccumulation by deep-sea organisms (1-3).Asimilar feature could be expected for organotin compounds due to their widely use, relatively high affinity for particulate matter, which makes sediments a major reservoir for these pollutants, and elevated half-life in deep-sea anoxic sediments (4). However, despite available monitoring data for coastal and shallow environments (5- 8), few works have addressed the contamination of deep-sea areas (9) and the uptake of those compounds by inhabiting organisms (10).
FIGURE 1. Map of the NW Mediterranean showing the locations of the sampling sites (grey area). Collections carried out at 42°35'N 4°07'E, 42°28'N 4°06'E, 41°14'N, 1°58'E.
Organotin compounds are used worldwide not only as biocides in antifouling paints but also as preserving agents for wood and timber, fungicides in agricultural activities, heat and UV stabilizers of PVC, and as catalyst in the production of polyurethane foams (11). The application of trialkyltin compounds as biocides, fungicides, and alguicides results in direct release into the water, with the consequent uptake and accumulation in aquatic fauna. Earlier studies have demonstrated that tributyl-and triphenyltin compounds exert chronic toxic effects on susceptible mollusks at water concentrations of a few nanograms per liter (12). Their acute toxicity to fish embryonic and early life stages lies in the range of 7-10 µ/L (11). Concern over the ecotoxicological impacts of TBT lead in the early 1990s to restrict its application to large vessels (>25 m long) in most developed countries. However, up to date, there is no regulation on the use of triphenyltin (TPT), neither in antifouling paints nor in agriculture.
The area of study, the NW Mediterranean, has suffered a great touristic development in the past decades, with a consequent increase in the number of marinas, considerable commercial ship traffic, and an augment of the TBT input into the marine environment in some areas (13). Nowadays, TBT contamination is certainly not limited to harbors and marinas but extends along the coast (5, 6), including protected areas in Corsica (14) and organisms collected in the open sea, e.g. tuna fish and marine mammals (15, 16).
Hence, the present study attempted to determine residue levels of organotin compounds in five species of deep-sea fish (Mora moro, Lepidion lepidion, Coryphaenoides guentheri, Alepocephalus rostratus, and Bathypterois mediterraneus) from the Gulf of Lions-NW Mediterranean-collected at a depth between 1000-1800 m, with the aim of elucidating the status of contamination of the deep-sea environment by using fish as sentinel organisms. Chemical analysis were carried out in several fish organs: gills, digestive tube, liver, and muscle, which play a key role in the uptake, distribution, detoxification, and storage of pollutants.
Material and Methods
Sample Collection. Fish samples were collected by trawling in April 1996 from the Gulf of Lions (NW Mediterranean) at a depth ranging between 1000 and 1800 m (Figure 1, Table 1). Once on board, fish organs were immediately dissected, wrapped in clean aluminum foil, and stored at -20 °C. Samples were preserved for up to 6 months before their analysis.
TABLE 1. Sample Depth and Biological Data of Collected Specimens
organisms common name depth (m) weight (g) length (cm) CF a (g/cm3) M. moro Common mora 1008-1146 556±46 41.2±1.4 0.79±0.02 L. lepidion Mediterranean codling 1161-1615 57.3±4.9 22.6±0.6 0.52±0.02 C. guentheri Günther's grenadier 1008-1153 26.9±2.5 22.0±0.7 0.27±0.01 A. rostratus Risso's smooth-head 1146-1593 168±37 28.3±1.8 0.72±0.06 B. mediterraneus Spiderfish 1548-1816 15.0±2.2 14.9±0.5 0.44±0.04 aCF= condition factor calculated as [weight/ (length)3] x 100. Values are mean ± SEM ( n=6).
Organotin Analysis.
The analysis were based on those described by Morcillo et al. (5). Briefly, frozen samples were thawed, and the organs of two individuals were pooled and cut into small pieces. Afterward samples (1-2 g wet wt) were digested with 20% tetramethylammonium hydroxide for 2 h at 60 °C. After the digestion step, pH was adjusted to 5.0 with 2.0Msodium acetate-acetic buffer, and the following reagents added to the buffered solution subsequently: 4mL of freshly made 2% sodium tetraethylborate as the ethylation agent, 10 mL of n-hexane, and 50-100 ng of tetrabutyltin and tripentyltin as internal standard. The sample was shaken for 45 min, the hexane layer was collected, and the aqueous phase was extracted again twice with n-hexane. The combined organic phase was reduced to approximately 1 mL, passed through a 5% water deactivated alumina column (5 g), and eluted with 10 mL of n-hexane to remove lipids. The final extract was injected into a gas chromatograph coupled with a flame photometric detector (GC-FPD). A fused silica capillary column (30 m length × 0.25 mm; DB-17) was used for GC separation. The operating conditions were as follows: injector and detector temperature 280 °C, column temperature programmed from 60 to 280 °C at a rate of 10 °C/min, 10 min at 280 °C. The carrier gas was hydrogen (50 cm/s). Organotin compounds were identified by assigning peaks in samples to the corresponding peaks of external standard. Peak areas of individual organotin compounds were used for the quantification, and results were corrected for the recovery of the internal standard (92-104%). The limits of quantifications determined as 3 times baseline noises were 1.0 ng/g wet wt as Sn for butyltins and triphenyltin metabolites and 1.4 ng/g for triphenyltin. Procedural blanks were processed with every set of samples, and they were all free from organotin contamination or other interferences. The accuracy of the analytical method was checked using a certified reference biological material (NIES-11), being the recovery of TBT of 71%±3 (n > 10). Concentrations were normalized to Sn for comparative purposes.
Selected samples were analyzed for confirmatory identifications by computerized gas chromatography-mass spectrometry (GC-MS). The instrument was a Fisons 800GC interfaced to a Fisons MD 800 MS. Helium was the carrier gas at 30 cm/s. The GC oven temperature was programmed as above. The ion source, injector, and transfer-line temperatures were set at 200, 270, and 290 °C, respectively. All injections were in the splitless-mode with the split vent closed for 30 s. The mass spectrometer was operated in the electron ionization mode, and the mass range was scanned from 50 to 600 u at 0.5 s/scan.
Results and Discussion
Biological Data of Samples. Main characteristics of the analyzed fish are given in Table 1. Individuals were adults and samples homogeneous (fish size and weight). The condition factor (CF) was calculated as a general measure of the nutritional status (17). The highest CFs (0.72-0.79) were recorded for A. rostratus and M. moro, which indicates a better nutritional state of these organisms. The lowest CF (0.27) was detected in C. guentheri, a species adapted to live at greater depths, with maximum abundance at 1600-2200 m (18).
Species Differences.
Organotin levels differed greatly among species (Table 2). The highest butyltin and phenyltin residues were recorded in the liver of M. moro (174 and 1668 ng/g wet wt as Sn, respectively) followed by L. lepidion (43 and 260 ng/g wet wt as Sn), both species from the moridae family. The lowest residues were detected in A. rostratus (5 ng of butyltins/g wet wt in the liver).
The uptake of butyl- and phenyltin compounds through the gills was particularly high in M. moro and L. lepidion (Table 2). Both organisms are large demersal species that swim actively in the upper slope (1000-1400 m), and this might lead to a relatively high and similar uptake of pollutants through the gills. Interestingly, Michel and Averty (9) reported a TBT contamination peak of 0.04 ng/L as ion (0.02 ng/L as Sn) at 1200min deep-waters from the area, that progressively reduced down to 2500 m depth. In contrast, butyl- and phenyltin residues were close to or below detection limit in the gills of the other three species examined. The reduced motility of these species, particularly B. mediterraneus and C. guentheri, and the fact that they are well adapted to live at greater depths, with a maximum abundance at 1600- 2200 m (18), would probably account for the very low or undetectable uptake of organotin compounds through the gills.
The organotin compound uptake through the diet was high in M. moro, followed by L. lepidion and B. mediterraneus, while organotin residues were below detection limit in digestive tube of A. rostratus and C. guentheri (Table 2). The results are again indicative of different habitats and patterns of exposure. In general terms, those organisms that feed actively, either on small fish, crustaceans, and cephalopods (M. moro) or on copepods and small decapods (L. lepidon) (19), exhibited high organotin residues in digestive tube. In contrast, those with a very specialized diet, such as A. rostratus, a large fish which feeds predominantly on gelatinous macroplankton, had residues below detection limit. B. mediterraneus, a sedentary fish, well adapted to the oligotrophic deep environment, which feeds on zooplankton carried by the marine currents (20), showed relatively higher uptake of organotin compounds through the diet than through the water.
Although there is increasing information on the composition and variability of the diets of deep-sea fish (18-20), no data on organotin concentrations on their prey species are available. Rough estimates on the food chain magnification of organotin compounds in M. moro and L. lepidon can be obtained by dividing the concentration in the whole body and the concentration in their digestive tube. This putative biomagnification factor (BMF) ranges for TBT from 0.02 in M. moro to 0.04 in L. lepidion, whereas for TPT goes from 0.27 in M. moro to 0.93 L. lepidion. These values are in the lower range of those described previously in fish (9, 20), and they clearly indicate the biodegradable nature of TBT in comparison with TPT in the food chain.
Patterns of Occurrence. Both butyl- and phenyltin compounds were recorded in muscle (<1-6 ng/g), gills (<1- 38 ng/g), and digestive tube (<1-50 ng/g), but they were particularly abundant in the liver (5-1700 ng/g), where they accounted for 70-90% of total detected organotins. Tissue residues of phenyltins dominated over butyltins in some species and tissues, and both generally decreased in the order liver > digestive tube > gills > muscle.
TABLE 2. Organotin Residues in Deep-Sea Fish from the NW Mediterranean a
organism liver muscle gills digestive tube M. moro MBT 54.5±17.7 <1.0 <1.0 <1.0 DBT 67.0±15.2 <1.0 4.3±2.5 7.1±0.8 TBT 52.1±12.2 <1.0 15.2±2.3 16.4±2.4 MPT 152.4±34.1 <1.0 <1.0 <1.0 DPT 85.2±20.0 <1.0 <1.0 6.1±1.4 TPT 1430±63 3.5±0.8 38.5±7.2 43.0±7.2 L. lepidion MBT 9.7±4.1 <1.0 <1.0 0.9±0.0 DBT 27.2±12.4 <1.0 2.4±1.3 16.3±1.9 TBT 6.6±3.6 <1.0 2.5±1.4 6.0±1.0 MPT 49.2±22.0 <1.0 <1.0 <1.0 DPT 34.9±12.5 <1.0 <1.0 1.0±0.5 TPT 176.5±66.3 <1.4 35.3±35.3 7.3±0.6 C. guentheri MBT 2.8±2.8 <1.0 <1.0 <1.0 DBT 7.4±1.6 4.9±4.3 <1.0 <1.0 TBT 5.6±5.6 <1.0 1.4±1.4 <1.0 MPT <1.0 <1.0 <1.0 <1.0 DPT 12.7±1.8 <1.0 <1.0 <1.0 TPT 35.5±5.8 <1.4 <1.4 <1.4 A. rostratus MBT <1.0 <1.0 1.3±0.6 <1.0 DBT 4.0±2.1 <1.0 <1.0 <1.0 TBT 1.0±1.0 <1.0 <1.0 <1.0 MPT <1.0 <1.0 <1.0 <1.0 DPT <1.0 <1.0 <1.0 <1.0 TPT <1.4 <1.4 <1.4 <1.4 B. mediterraneus MBT b <1.0 <1.0 1.4±0.8 DBT b <1.0 <1.0 2.3±1.2 TBT b <1.0 1.2±1.2 18.9±1.4 MPT b <1.0 <1.0 <1.0 DPT b <1.0 <1.0 <1.0 TPT b <1.4 3.1±1.8 13.7±3.3 a Values are mean±SEM ( n=3), in ng/g wet wt as Sn. Each sample a pool of two organisms. bSample not available.
Regarding butyltins, TBT dominated over its metabolites (DBT and MBT) in both gills and digestive tube, whereas the opposite trend was observed in the liver. Hence, TBT/DBT ratios ranged from 0.24 to 0.78 in the liver and from 2.3 to 8.2 in digestive tube and gills of the species analyzed, with the exception of Lepidion lepidion (0.4-1.0). The prevalence of DBT in the liver (40-80% of total butyltins) was observed in all the studied species, irrespective of the liver concentration of butyltins, and this has also been reported in coastal fish (5) and marine mammals (15, 16) from the NW Mediterranean. A similar proportion of DBT (55-75% of total butyltins) has been reported in the liver of marine mammals from developed countries (21) and attributed to both breakdown of TBT and specific sources of DBT, namely, stabilizers of PVC and catalysts for some industrial processes. Among phenyltins, TPT strongly dominated over DPT not only in gills and digestive tube (87-100% of phenyltin residues; TPT/DPT > 7.0) but also in the liver (70-85% of phenyltin residues; TPT/DPT ratios between 2.8 and 16.8).
The results indicate a certain ability of fish to metabolite TBT in contrast to TPT and a preferential accumulation of TPT in the liver. In general, trialkyltin compounds are known to bind to amino acids, peptides, and proteins (22), and this complexation between TBT or TPT and metal-binding proteins may influence tissue distribution (23). Additionally, bioaccumulation depends on other factors, viz. habitat, dietary uptake, pollutant bioavailability, and biotransformation (24). In deep-sea fish, TBT enters via food (<1-19 ng/g) or it is adsorbed through the gills (<1-15 ng/g) in contact with seawater, and it is rapidly metabolized in the liver, where it represents 2-9% of the total organic tin detected. In contrast, the uptake of TPT via food (<1-43 ng/g) or water (<1-38 ng/g) is similar or slightly higher than the uptake of TBT, but this compound is hardly metabolized in the liver, where it represents 55-78% of total organic tin. These results are consistent with data on shallower species that indicated higher biomagnification factor, percentage of retention, and assimilation efficiency of TPT in comparison with TBT and a slower excretion rate of the former (25).
Contamination Status. To understand the current status of organotin pollution in deep-sea fauna, residue levels found in our samples were compared with those of other species collected in harbors, coastal, and open-sea areas from the NW Mediterranean. Total butyltin (MBT + DBT + TBT) residues, which in this study ranged from 5 ng/g in the liver of A. rostratus to 175 ng/g in M. moro, were comparable to those found in coastal fish collected along the Catalan coast (2-34 ng/g as Sn) (5), and in the range of those reported in deep-sea fish from Suruga bay (Japan) (20-580 ng/g wet wt of TBT as ion; 9-247 ng/g wet wt as Sn) sampled between 220 and 740 m depth (10). Figure 2 summarizes TBT concentration in different organisms collected in the NW Mediterranean area (5, 6, 15, 26). Despite the decrease in TBT body residues in deep-sea fish, in relation to organisms collected in harbors and coastal areas, the present work evidences the expansion of butyltin contamination to the deep-sea environment and the uptake of those compounds by deep-sea fauna. Additionally, the TBT residues recorded in deep-sea organisms (see Table 2) were between reported values of estimated effective concentrations (20-100 ng/g wet wt as ion; 8-40 ng/g wet wt as Sn) based on chronic toxicity endpoints in molluscs (27, 28). Other studies indicated that TBT and TPT exert cytotoxic effects in fish hepatoma cells at nanogram per gram levels (29). Based on this information, it is plausible that deep-sea organisms are affected by butyltin contamination.
Total phenyltin (MPT + DPT + TPT) concentrations ranged from <4 ng/g in the liver of A. rostratus to 1667 ng/g in M. moro. The residues observed in some of these species are much higher than those reported in coastal fish from the area (8-73 ng/g as Sn) (5). The tendency of TPT to accumulate in marine organisms was first noticed by Takami et al. (30); the authors found that although the annual production of TPT in Japan was about one-tenth that of TBT, TPT residues in biota samples were higher than TBT. Since then, an increasing number of studies have reported TPT residues in biota samples. High concentrations of phenyltins have been determined in the hepatopancreas of horsecrabs, Tachaaypleus tridentatus, collected from Japanese coastal waters (28-4200 ng/g wet wt as Sn), which were on average, 2-fold higher than those of butyltins (31). Harino et al. (32) reported concentrations of TPT of 0.3-44 ng/g wet wt in muscle of fish from Japan and higher concentrations in the liver (17- 75 ng/g wet wt as Sn).
FIGURE 2. TBT concentration in different organisms collected in the NW Mediterranean area. Results in ng/g wet wt as Sn. Data from refs 5, 6, 15, and 26.
FIGURE 3. TPT concentration in different organisms collected in the NW Mediterranean area. Results in ng/g wet wt as Sn. Data from refs 5, 6, and 26. Top left figure: Main figure with data from M. moro included.
The first report of TPT in Mediterranean coastal samples was published by Tolosa et al. (33); TPT was detected in marina samples, and the authors infer that contamination probably arose from the antifouling paints of small boats. Since then, TPT has been detected in Monaco port (34), in French coastal waters in 1992 and 1997 (7), and in molluscs and fish from the Catalan coast (5-6). A recent work by Díez et al. (13) indicates that TPT is probably no longer used in antifouling paints, as the degradation products (DPT and MPT) strongly dominate over TPT in water and sediment samples collected from several Mediterranean harbors. Hence, the use of TPT as a fungicide in agriculture or as an algaecide in rice fields can be alternative sources of the compound into the aquatic environment.
Whatever the source is, the transport of TPT to the deep-sea environment is not unlikely. Volatilization is reported to be an important transport route for this compound, that has been reported in rainwater at remote locations (35). Additionally, sediment-water partition coefficient (Kd) of TPT varies between 21 and 113 × 103 L/kg, whereas for TBT Kd fluctuates between 1 and 3.0 × 103 L/kg (11). These values determine the presence of TBT both in water and particulate material, whereas TPT will be mainly associated to particulate material, and, therefore, transport processes to deep-sea areas could be comparatively more important for TPT than for TBT. Besides, the fact that many of the deep-water fish species are long-lived and tend to feed at higher trophic levels than their shallow-water counterparts (36)maylead to a potentially higher level of accumulation of persistent pollutants, particularly those that are not easily metabolized or degraded, as is the case of TPT.
Figure 3 compares TPT levels in deep-sea fish, with those in shallow-water organisms from the region (5, 6), and shows the elevated contamination detected in deep-sea fauna and the need to further investigate the extent of this contamination and the impact of phenyltin compounds in the bathayal and abyssal fauna. The extreme conditions of deep-sea environments (high pressure, low temperature, and absence of sunlight) may reduce both biotic and abiotic degradation of organotin compounds, resulting in a longer persistence (4, 37-39), and this effect could be even more evident for TPT.
Overall, this work shows that organotin pollution in the NW Mediterranean is not limited to circumscribed coastal areas but reaches the deep-sea environment and inhabiting organisms (1000-1800 m depth). To our knowledge, this is the first report on the detection of phenyltin compounds in deep-sea organisms. Special attention should be paid to the unusually high TPT levels found in deep-sea fauna and their potential adverse effects on deep-sea ecosystems.
Acknowledgments
Veronica Borghi acknowledges a predoctoral grant of the Catalan Government (Generalitat de Catalunya). The authors are thankful to Amaya Albalat for her valuable help in sample processing and to Dr. Montserrat Solé, Dr. Francçois Galgani, and the crew of the IFREMER boat "Europe" for making the sampling possible. We are also grateful to two anonymous referees for their useful comments to the manuscript.
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Received for review April 17, 2002. Revised manuscript received July 8, 2002. Accepted July 17, 2002.
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