Article pubs.acs.org/est
Evidence of Butyltin Biomagnification along the Northern Adriatic Food-Web (Mediterranean Sea) Elucidated by Stable Isotope Ratios Tomaso Fortibuoni,* Seta Noventa, Federico Rampazzo, Claudia Gion, Malgorzata Formalewicz, Daniela Berto, and Saša Raicevich Italian National Institute for Environmental Protection and Research (ISPRA), Loc. Brondolo, 30015 Chioggia (VE), Italy S Supporting Information *
ABSTRACT: The biomagnification of tributyltin (TBT), dibutyltin (DBT), monobutyltin (MBT), and total butyltins (ΣBT) was analyzed in the Northern Adriatic food-web (Mediterranean) considering trophodynamic interactions among species and carbon sources in the food-web. Although it is acknowledged that these contaminants bioaccumulate in marine organisms, it is still controversial whether they biomagnify along food-webs. A wide range of species was considered, from plankton feeders to top predators, whose trophic level (TL) was assessed measuring the biological enrichment of nitrogen stable isotopes (δ15N). Carbon isotopic signature (δ13C) was used to trace carbon sources in the food-web (terrestrial vs marine). At least one butyltin species was detected in the majority of samples, and TBT was the predominant contaminant. A significant positive relationship was found between TL and butyltin concentrations, implying food-web biomagnification. Coherently, the Trophic Magnification Factor resulted higher than 1, ranging between 3.88 for ΣBT and 4.62 for DBT. A negative but not significant correlation was instead found between δ13C and butyltin concentrations, indicating a slight decreasing gradient of contaminants concentrations in species according to the coastal influence as carbon source in their diet. However, trophodynamic mechanisms are likely more important factors in determining butyltin distribution in the Northern Adriatic food-web.
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INTRODUCTION
banning the use of TBT-based paints since 1 January 2003, and its total prohibition since 1 January 2008. Despite the ascertained decrease of butyltins (BT) environmental levels fostered by the global ban of TBT, they are still found in the marine compartment.6,7 Indeed, these widely distributed contaminants are highly persistent, and contaminated sediments represent the main long-term secondary source of contamination to the water column, since the adsorption of TBT to sediments is reversible.1 Important issues related to BT fate in aquatic environments are still under debate. Among these, the uncertainties about their biomagnification processes along marine food-webs (concentration increase in an organism relative to its diet, due to uptake from food) are considered relevant knowledge lacks, being humans at the top of the trophic web. It is well established that, once released into the water, TBT tends to be absorbed by suspended particulate organic matter (POM)6 due to its hydrophobicity, and then it enters in the food-web via assimilation by zooplankton and grazing benthic invertebrates. TBT bioaccumulation, in fact, has been reported in all trophic
Organotin compounds (OTC) have been used worldwide as biocides in antifouling paints for more than three decades. In particular, tributyltin (TBT) by-design release from ship hulls and submerged structures has historically represented the most important source of OTC in the marine environment, even if there are further inputs derived from other applications, i.e. as fungicide in agricultural activities, wood preservative, industrial catalyst in the production of polyurethane foams, and stabilizer in the synthesis of polyvinyl chloride (PVC).1,2 TBT, as well as its breakdown products (dibutyltin (DBT) and monobutyltin (MBT)), are noted to exert toxic effects also on various nontarget marine organisms.2 Among the most acknowledged chronic effects there are the shell thickening in the Pacific oyster (Crassostrea gigas)3 and the exhibition of sexual male characteristics in female gastropods (Imposex− Intersex).4 OTC were also shown to be genotoxic and act as an endocrine disrupter in fish, and to increase the risk of cancer and immunotoxicity in humans.5 Due to high toxicity, use of TBT in antifouling paints has been limited in many countries since the mid-1980s, and was finally prohibited by the entry of AFS (Anti-Fouling System) Convention, the agreement promoted by the International Maritime Organization (IMO) that called for a global treaty © 2013 American Chemical Society
Received: Revised: Accepted: Published: 3370
November 29, 2012 February 21, 2013 March 6, 2013 March 6, 2013 dx.doi.org/10.1021/es304875b | Environ. Sci. Technol. 2013, 47, 3370−3377
Environmental Science & Technology
Article
levels, from shellfish, squid, and fish, to top predators such as whales, dolphins, seals, and piscivorous birds.1,8,9 However, there is a general scarcity of studies assessing BT biomagnification in marine food-webs, and those available provide contradictory evidence on this topic.1,10 The analysis of the biomagnification profiles requires a sound knowledge of organisms’ trophic interactions. In this context, the stable nitrogen isotopic signature (δ15N, i.e. 15N/14N) of organisms’ tissues is recognized as one of the most reliable methods to assess the trophic level (TL) of species, since δ15N increases 3−4‰ in the passage between subsequent TLs.11 Also δ13C (13C/12C) can be used to this purpose (increasing of 1‰ with an increase of one trophic level),10 even if the carbon isotopic signature is preferentially employed to provide clues about the origin of carbon in the consumers’ food.12 Differences of δ13C values in consumers at increasing distance from the coast are, in fact, explained as the progressive decrease of the terrestrial influence on the marine compartment as carbon sources in diet. This assumption is based on the evidence that terrestrial primary producers have lower (more negative) δ13C values than marine ones, and this pattern is reflected also in organisms feeding mainly on preys whose diet is linked to terrestrial organic carbon for growth.13 This study aimed at assessing BT biomagnification process in the Northern Adriatic food-web (Mediterranean Sea) considering trophodynamic interactions among species and carbon sources in the food-web through stable isotopes analysis. It was assumed that a negative relationship between carbon isotopic signature and contaminant tissues concentrations should be observed since historical TBT hot spots are mainly located close to the coast (i.e., areas characterized by high shipping density, such as harbors, marinas, and docks).2,6,14 The Trophic Magnification Factor (TMF)15 of BT was computed for assessing biomagnification in the food-web. Organotin concentrations were determined in muscle and liver/ hepatopancreas samples separately and not in the whole body to obtain information on their partitioning between muscle and liver tissues. Furthermore, this choice allows to know the current levels of BT in the edible parts (i.e., white muscle) of commercial species, and thus to collect information relevant in terms of human dietary exposure to these contaminants.
Figure 1. Map of the Northern Adriatic Sea area (N Mediterranean Sea) where samples were collected. Sampling sites: red triangles, sites where dead specimens of common bottlenose dolphin were found beached; blue squares, sampling locations of fish and invertebrates (commercial fishing vessels); black circles, sampling locations of fish and invertebrates (“SoleMon” trawl-survey).
included in the analysis in order to represent the possible link between detritus and the pelagic food-web. Twenty six species, representative of a wide range of trophic levels (from plankton feeders to top predators), were investigated in this study. The list of species is reported in Table S1 (Supporting Information). It includes four invertebrate species, eighteen bony fish species, three cartilaginous fish species and one mammal species, for a total of forty four samples. All fish and invertebrates samples were collected on board fishing vessels using different gear (i.e., midwater pelagic trawls, beam trawls, trammel nets) and during the “SoleMon” trawlsurvey. Tissues of common bottlenose dolphins (Tursiops truncatus) were provided by the Mediterranean Marine Mammal Tissue Bank, Department of Experimental Veterinary Science, University of Padua (Italy). Samples were dissected from dead specimens beached along the NAS coast (still fresh tissues or minimally decomposed). Zooplankton samples were collected by vertical tows (bottom to surface, 335-μm mesh size) in order to use zooplankton δ15N value to characterize the food-web baseline in the computation of the TL of species. Samples of muscle and liver/hepatopancreas were dissected from each specimen. In fishes muscle samples were taken from the dorsal muscle (white muscle), above the pectoral fin and the ocular side. When collected specimens were too small to obtain a quantity of tissue allowing chemical analyses (∼ 20 g wet weight), each sample consisted of pooled filets from 3 to 20 individuals homogeneous in size and origin (sampling site) (Table 1). Once collected, all samples were homogenized, lyophilized, and kept in the darkness at −20 °C until the analysis. Stable Isotopes Analysis. Isotopes analysis was carried out on muscle samples. This tissue is characterized by low isotopic turnover20 and scarce variability in δ13C and δ15N, reflecting the feeding habits over longer periods than liver samples.21 Furthermore, δ15N values of muscle are considered to more closely reflect those of the whole body than do other tissues.22 Lipids were extracted before analyzing carbon isotopes (13C and 12C) according to the Folch method modified by Boscolo
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MATERIALS AND METHODS Sample Collection. Sampling activities were carried out between 2008 and 2010 in the Northern Adriatic Sea (NAS), a shallow (average depth of 33.5 m) and semienclosed basin located in the northern part of the Mediterranean Sea (Figure 1). When assessing behavior of contaminants, it is important to study well-known food webs.16 The NAS food-web is well studied, and species included in this work were selected considering well-defined trophic relationships according to studies on diet composition of Mediterranean species,17 trophic mass-balance models referred to the Adriatic Sea,18,19 and expert knowledge. Species showing trophic relevance in the food-web (i.e., keystone species, such as crabs, anchovies, sardines, and dolphins)18,19 and species important as seafood resources (e.g., common cuttle-fish, brill, European flounder, gilthead seabream, Atlantic horse mackerel) were considered as well. Furthermore, since an important coupling between the pelagic and demersal compartments was observed in the NAS,19 and sediments may act as a long-term secondary source of contamination, also benthic and demersal species were 3371
dx.doi.org/10.1021/es304875b | Environ. Sci. Technol. 2013, 47, 3370−3377
Environmental Science & Technology
Article
Table 1. TBT, DBT, and MBT Concentrations (ng Sn g−1 d.w.) in Muscle and Liver Samples Collected in the NASa muscle phylum crustaceans cephalopods
bony fish
elasmobranchs
mammals
liver
species
common name
TBT
DBT
MBT
TBT
DBT
MBT
δ15N
δ13C
no. of individuals
Liocarcinus depurator Liocarcinus vernalis Eledone moschata Eledone moschata Sepia of f icinalis Sepia of f icinalis Sepia of f icinalis Sepia of f icinalis Chelidonichthys lucerna Dicentrarchus labrax Dicentrarchus labrax Engraulis encrasicolus Lichia amia Liza ramada Merlangius merlangus Merluccius merluccius Mullus barbatus Mullus surmuletus Platichthys f lesus Sarda sarda Sardina pilchardus Sardina pilchardus Scomber japonicus Scomber scombrus Scophthalmus rhombus Scophthalmus rhombus Solea solea Solea solea Solea solea Solea solea Sparus aurata Trachurus trachurus Trachurus trachurus Mustelus mustelus Mustelus mustelus Prionace glauca Prionace glauca Raja spp. Tursiops truncatus Tursiops truncatus Tursiops truncatus Tursiops truncatus Tursiops truncatus Tursiops truncatus
blu-leg swimcrab gray swimmingcrab musky octopus musky octopus common cuttlefish common cuttlefish common cuttlefish common cuttlefish tub gurnard European seabass European seabass European anchovy leerfish thinlip gray mullet whiting European hake red mullet striped red mullet European flounder Atlantic bonito European pilchard European pilchard chub mackerel Atlantic mackerel brill brill common sole common sole common sole common sole gilthead seabream Atlantic horse mackerel Atlantic horse mackerel smooth-hound shark smooth-hound shark blue shark blue shark rays common bottlenose dolphin common bottlenose dolphin common bottlenose dolphin common bottlenose dolphin common bottlenose dolphin common bottlenose dolphin
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