Tissue distribution of triphenyltin compounds in marine teleost fishes

Highlights

• TPT was found to exhibit a preferential distribution pattern in fish tissues.

• TPT has a higher affinity to proteins than lipids in fish tissues.

• Highest and lowest TPT concentrations occurred in liver and scales, respectively.

• Dorsal and ventral muscles can best estimate the TPT burden in the entire fish.

Abstract

Continuous release of the highly toxic triphenyltin compounds (TPT) from antifouling paints and fungicides has caused serious pollution to urbanized coastal marine environments worldwide since the 1960s. Using gas-chromatography mass-spectrometry (GC–MS), this study investigated the distribution profile of TPT in 15 types of tissues of four marine teleost fish species collected from Hong Kong waters. Concentrations of TPT in various tissues had a significant positive correlation with protein contents in the tissues (r = 0.346, p < 0.001) and, to a lesser extent with lipid contents (r = 0.169, p =  0.020). Highest concentrations of TPT were consistently found in liver, ranging from 1074.9 to 3443.7 ng/g wet weight; whereas fish scales always contained the least concentration of TPT in all species, ranging from 10.4 to 48.5 ng/g wet weight. Through mass balance models and regression analyses, muscle tissues were found to contribute most to the total TPT body burden, and the average TPT concentration of both dorsal and ventral muscles was identified as the best predictor for estimating TPT burden in the entire fish. Hence, further investigations of bioaccumulation and biomagnification of TPT in fishes should adopt this modelling approach in estimating its total body burden in individual fish.

Introduction

Among the known endocrine disrupting chemicals (EDCs), organotin compounds (OTs), especially triphenyltin (TPT) compounds, are considered the most toxic and prevalent EDCs detected in the marine environment along the coast of South China region (Chen et al., 2019; Goldberg, 1986). Even though the use of these compounds in antifouling paints have been banned by the International Maritime Organization in 2008 (IMO, 2008), these compounds are still detectable in the region. For example, TPT concentrations in the marine environment of Hong Kong were 3.8–11.7 ng/L, 71.8–91.7 ng/g dry weight, and 9.6–1079.9 ng/g wet weight in seawater, sediments, and biota, respectively (Sham et al., 2020a). These notorious compounds not only can cause immunotoxic and neurotoxic effects to marine organisms (Doherty and Irwin, 2011; Fent, 1996), but also potent endocrine disrupting effects that can subsequently impair their development and reproduction (de Araújo et al., 2018). TPT, in particular, has been proven to reduce fitness of marine organisms through a variety of ways: development of male sexual characteristics, including vas deferens and penis, in female gastropods (Davies and Smith, 1980); suppression of gametes production in both male and female fishes (Sun et al., 2011; Zhang et al., 2008); deformation of body parts (Hu et al., 2009), and reduction in swimming abilities in fishes (Yi and Leung, 2017). These adverse impacts on organisms can be transgenerational, as demonstrated in the marine medaka (Oryzias melastigma) that the unexposed fish of F1 generations from exposed parents were found to have abnormalities in survival, growth, fecundity and fertility (Horie et al., 2017; Sun et al., 2011). Therefore, elevated levels of TPT may cause negative impacts on fish populations and thereby threaten the community of the marine ecosystem (Sun et al., 2011).

While toxicodynamics of TPT in marine fishes have been extensively studied, studies on toxicokinetics of TPT such as their exposure routes, transportation and storage within the fish body, remain scarce (Evans, 2013). This information regarding the toxicokinetics of EDCs can be generally elucidated through revealing the tissue-distribution profile in fish that has experienced long-term exposure in the wild (Renwick, 2006; Shi et al., 2015). Such a profile is governed by both the allocation of lipophilic and hydrophilic components in the organism, as well as the chemical properties of the EDC (Weisbrod et al., 2000). Though TPT is considered lipophilic because of its relatively low solubility in water (Rüdel et al., 2003; WHO, 1999; Yi et al., 2012), the “ionic-covalent” bonding between carbon and tin in TPT also yields its affinity to proteins and glutathione (Appel, 2004; Rose and Aldridge, 1968). Such contrasting chemical properties of TPT may result in a different tissue distribution profile in fishes when compared to other lipophilic EDCs, which may consequently affect its toxicokinetics in fishes. In particular, the relatively low lipophilicity of TPT suggests that these compounds may not be able to biomagnify along the food web (Borgå et al., 2012). Yet, Sham et al. (2020b) have recently discovered that marine dolphins and porpoises inhabiting the adjacent waters of Hong Kong consistently contain the highest concentration of TPT in comparison to their preys, and TPT can be biomagnified via the marine food web. Similar findings were also reported in the food web of seals in the Fildes Peninsula coast of Antarctic (He et al., 2018). Furthermore, the tissue-distribution profile of TPT allows estimations of the relative contribution of individual tissues to the total TPT body burden (Yamada et al., 1994), thus deriving appropriate proxies to estimate total body burden of TPT in the whole organism (Yordy et al., 2010).

A comprehensive description of tissue-specific accumulation of TPT and its degradation products (mono- and di-phenyltin; MPT and DPT), collectively known as phenyltin compounds (PTs), however, is still lacking in fishes. Limited studies attempted to assess the accumulation pattern of TPT in tissues of fishes; the majority of which only accounted for three to four major tissues including dorsal muscles, stomach, gills, and liver (Albalat et al., 2002; Lee et al., 2005; Morcillo et al., 1997; Ohji et al., 2007). Therefore, this study aimed to (1) construct the TPT distribution profile in 15 different tissues of four selected marine teleost fishes; (2) reveal the relationship between tissue concentration of TPT and lipid or protein contents in the studied fishes; (3) extrapolate the tissue distribution profile of TPT to deduce the total TPT burden in the whole fish through an integrative use of mass balance models and regression models. The results obtained in this study, when synthesized with the knowledge of biodegradation products and metabolic processes of TPT compounds in the fish body, will be critical to further determine bioaccumulative properties and biomagnification potential of these compounds in the marine ecosystem.