Contaminant screening and tissue distribution in the critically endangered Brazilian guitarfish Pseudobatos horkelii

https://doi.org/10.1016/j.envpol.2020.114923Get rights and content

Highlights

  • Trace metals, PAHs and emerging contaminants were determined in a guitarfish.

  • Contaminants are tissue-specific, and the highest levels were found in liver.

  • PAHs and diclofenac had the highest concentrations.

  • PAHs and dichlofluanid in muscle are associated with chronical exposure.

  • P. horkelii is exposed to environmental contamination in southern Brazil.

Abstract

Elasmobranchs are particularly prone to accumulating contaminants due to their life history patterns and relatively high trophic position. However, several compounds, especially contaminants of emerging concern, have still not been well studied in this group. Here, we aimed to determine the occurrence and concentrations of several inorganic and organic contaminants in different tissues of the Brazilian guitarfish Pseudobatos horkelii. This species is a critically endangered species, endemic from the Southwest Atlantic which uses southern Brazilian waters as a nursery habitat. Polycyclic aromatic hydrocarbons (PAHs), emerging pesticides, pharmaceutical and personal care products (PPCPs) and trace metals were determined in five biological tissues in order to assess the accumulation and organotropism of these compounds. Except for chlorothalonil and triclosan, all compounds were detected in, at least, one tissue, mostly in liver samples. All compounds differed among tissues, with liver presenting the higher concentrations of several contaminants, followed by muscle and gills. PAHs and PPCPs were the most detected analytes and presented the highest concentrations among tissues. Diclofenac levels were determined, for the first time in elasmobranchs, and were relatively high, when compared to other fishes. Finally, relatively high concentrations of PAHs, dichlofluanid and octocrylene in muscle might be suggestive of chronic exposure, presenting also human health implications. Regarding trace metals, contrary to most elasmobranch studies, Hg levels were low in all tissues, whereas Cd and Pb here higher in liver, and gills and blood samples, respectively. Our results indicate that P. horkelii is exposed to several organic and inorganic which might affect this species in a long-term scale. Concerning the determination of emerging contaminants, it is likely that other elasmobranchs are also exposed to these compounds and special attention should be given to this issue in order to predict future effects on this group.

Introduction

For the past decades, several compounds were considered as major contaminants in coastal regions due to their persistency and potential deleterious effects on organisms (Fleeger et al., 2003). On the other hand, a variety of newly synthesized compounds, considered as of emerging concern (CE), such as pharmaceuticals and personal care products (PPCPs), has been recently determined in marine ecosystems (Arpin-Pont et al., 2014). These compounds lack of monitoring and are potentially harmful to aquatic environments and wildlife (Sauvé and Desrosiers, 2014; Zenker et al., 2014). Whereas trace metals and legacy contaminants are persistent in the environment and prone to accumulate in marine wildlife, CEs are generally considered pseudo-persistent due to their indiscriminate use and chronic release in aquatic systems (Boxall et al., 2012; Overturf et al., 2015), despite their relatively rapid degradation. Yet, little is known on their occurrence and potential to accumulate in marine species. Impacts of CEs have already been hypothesized to be associated with population declines in birds (Oaks et al., 2004), and femininization of freshwater fishes with consequences at a population-level (Kidd et al., 2007), but studies conducted on marine species are mostly limited by experimental designs on traditional model species (Dann and Hontela, 2010; Fabbri and Franzellitti, 2016).

Elasmobranchs tend to accumulate high levels of contaminants due to their higher trophic positions, acting as meso and apex predators, and life history parameters, such as longevity. Accumulation of legacy contaminants and trace metals has been extensively studied among this group (Gelsleichter and Walker, 2010), whereas studies evaluating CEs are incipient, with only a few compounds being analyzed (Gelsleichter and Szabo, 2013; Lyons et al., 2018; Nakata, 2005; Nakata et al., 2009; Xue and Kannan, 2016; Xue et al., 2017). However, due to their trophic proximity, as well as k-strategy life-history patterns, with other taxa in which PPCPs have been detected (Gago-Ferrero et al., 2013; Fair et al., 2009; Nakata, 2005), it is highly expected to also detect these compounds and its metabolites in elasmobranch tissues. Regarding tissue distribution, a few studies have evaluated the distribution of contaminants (De Boeck et al., 2010; Corsolini et al., 2014), but are still scarce, especially considering CEs. For this reason, studies analyzing organotropism of contaminants are determinant for understanding the kinetics and associated physiological impacts of environmental contamination in elasmobranchs.

The Brazilian guitarfish Pseudobatos horkelii is a bottom-dweller endemic species from the Southwestern Atlantic occurring from southeastern Brazil to Argentina (Menni and Stehmann, 2000). This species shows a synchronous reproductive cycle, with pregnant females approaching shallow waters during the summer for embryonic development and parturition (Lessa et al., 1986; Martins et al., 2018). Southern Brazil represents a nursery area for southern populations, which are considered resident (Vooren et al., 2005). This species was categorized as “Critically Endangered” by the IUCN Red List of Threatened Species (Lessa and Vooren, 2016) and landing and commercialization are, therefore, prohibited by the Brazilian legislation (IBAMA, 2004). Despite this, P. horkelii is still illegally traded (De-Franco et al., 2012; Bunholi et al., 2018) and consumed, especially in southern Brazil.

Urban, industrial, agricultural and harbor activities have been impacting the southern Brazilian estuaries, mostly from inland sources (Mirlean et al., 2003; Wallner-Kersanach et al., 2016). The Patos Lagoon is the largest water body from South America and receives most of freshwater systems input, which are possible sources of contamination (Amado et al., 2006). This input of contaminants ends up in the marine environment, especially through the Rio Grande Channel. Caldas et al. (2019) detected several emerging compounds in surface and even drinking water from this area, suggesting that aquatic organisms might be exposed to emerging pesticides and PPCPs. Moreover, livestock and agricultural activities might also impact organisms in southern wetlands (Quintela et al., 2019), which run off to the coast. Considering this, it is likely that agricultural runoff, added to the already mentioned activities might also impact marine ecosystems and organisms, especially those inhabiting shallow waters.

In the light of the above, we hypothesize that P. horkelii might be exposed to environmental contamination of anthropogenic sources in southern Brazil. Furthermore, considering that its meat is illegally consumed, contaminant levels for this species are of great interest regarding human health. Taking this into account, we aimed to characterize, for the first time, the levels and tissue distribution of organic and inorganic compounds in five tissues of the Brazilian guitarfish P. horkelii, sampled in southern Brazil.

Section snippets

Study site

The Patos Lagoon is located in Rio Grande do Sul State, southern Brazil and has been receiving an input of contaminants from anthropogenic sources for about 15 years (Wallner-Kersanach et al., 2016). The southernmost estuarine region has been particularly affected due to an increase in port and naval activities, mostly in Rio Grande city (209,378 inhabitants, IBGE, 2017), where one of the largest harbors in southern Brazil is located. In addition, urban, industrial (fertilizer-producing plants,

Results and discussion

Descriptive statistics of concentrations of all organic contaminants in each tissue analyzed are provided in Table 1 and detection frequencies are provided in Table S4.

Conclusions

Our results indicate that P. horkelii is exposed to several contaminants in southern Brazil. Acute exposure was hypothesized to be related to liver levels whereas high concentrations in less metabolic tissues (e.g. muscle), especially of PAHs and emerging pesticides might reflect chronic exposure. However, high liver levels can also indicate chronic exposure and should not be only associated with acute exposure, since elasmobranchs are less efficient in xenobiotics metabolism in comparison with

Main findings

Pseudobatos horkelii is exposed to trace metals, polycyclic aromatic hydrocarbons and emerging contaminants and the highest levels were found in liver samples.

Notes

The authors declare no competing financial interest.

CRediT authorship contribution statement

Mariana F. Martins: Conceptualization, Formal analysis, Investigation, Writing - original draft, Writing - review & editing, Visualization, Funding acquisition. Patrícia G. Costa: Conceptualization, Methodology, Validation, Investigation, Writing - review & editing. Adalto Bianchini: Conceptualization, Resources, Writing - review & editing, Supervision.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) – Finance Code 001 and partially funded by the Save Our Seas Foundation (SOSF 422). A. Bianchini is a research fellow from the Brazilian Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq # 307647/20161). The authors thank the artisanal and recreational fisherman from Rio Grande, southern Brazil for donating the samples.

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