Negative metal bioaccumulation impacts on systemic shark health and homeostatic balance

Highlights

• Alterations in hepatic markers with the bioaccumulation of Co, Fe, and Hg in the liver of sharks were observed.

• Alterations in urea and lactate with the bioaccumulation of Fe and Hg in the gills of sharks were detected.

• Alteration in phosphorus with the bioaccumulation of Co, Mn, and Hg in the rectal gland of sharks was also observed.

• Body condition was influenced by metals, differing between males and females.

• Energy mobilization was influenced by metals, differing between adults and juveniles.

Abstract

Contamination by metals is among the most pervasive anthropogenic threats to the environment. Despite the ecological importance of marine apex predators, the potential negative impacts of metal bioaccumulation and biomagnification on the health of higher trophic level species remains unclear. To date, most toxicology studies in sharks have focused on measuring metal concentrations in muscle tissues associating human consumption and food safety, without further investigating potential impacts on shark health. To help address this knowledge gap, the present study evaluated metal concentrations in the gills, muscle, liver and rectal gland of coastal sharks opportunistically sampled from Brazilian waters and tested for potential relationships between metal bioaccumulation and general shark health and homeostatic balance metrics. Results revealed high metal concentrations in all four tissue types, with levels varying in relation to size, sex, and life-stage. Metal concentrations were also associated with serum biomarkers (urea, lactate, ALT, triglycerides, alkaline phosphatase, and phosphorus) and body condition, suggesting potential negative impacts on organismal health.

Introduction

As a taxonomic group, sharks are particularly vulnerable to anthropogenic stressors, such as exploitation, habitat degradation and climate change, due to life-history traits that feature late maturity and relatively low reproductive output (Gallagher et al., 2012; Worm et al., 2013; Pacoureau et al., 2021). While research into threats to sharks has primarily focused on mortality due to fishing, a growing concern on the possible sublethal impacts of bioaccumulated toxic pollutants (e.g., metals) on shark health and fitness is noted (Turoczy et al., 2000; Rumbold et al., 2014). While previous research has tested shark tissues for the presence and concentration of metals (e.g., Shipley et al., 2021), this has usually been addressed from a food safety perspective to ascertain whether metal levels would be safe for human consumption (e.g., Souza-Araujo et al., 2021; Hammerschlag et al., 2016; Anandkumar et al., 2018).

Some studies have evaluated the mechanistic consequences of metal contamination on shark physiological processes, including alterations in osmoregulatory function (Kinne-Saffran and Kinne, 2001; De Boeck et al., 2001, De Boeck et al., 2010; Grosell et al., 2003) as well as cellular and fluid composition (Ballatori and Boyer, 1996; De Boeck et al., 2001, De Boeck et al., 2010; Grosell et al., 2003). For example, Pb accumulation in the gills, rectal gland, muscle and liver has been shown to affect osmoregulation, respiratory capacity and energy metabolism in the dogfish shark (Squalus acanthias) (Eyckmans et al., 2013), while Ag and Cu accumulation in the gills, liver, kidney, rectal gland, intestine, muscle and skin tissues have been reported to cause respiratory disturbance, hyperventilation, blood alkalosis, altered anaerobic metabolism, lactate accumulation, erythrocyte swelling, and hemolysis in dogfish sharks (Scyliorhinus canicula and S. acanthias; De Boeck et al., 2001, De Boeck et al., 2010). Recently, Norris et al. (2021) evaluated mercury concentrations in blood, muscle, liver, and kidney samples from neonatal and juvenile blacktip sharks (Carcharhinus limbatus) in Southwest Florida. The study found that melanomacrophage presence and lipid deposition exhibit a significant association with Hg concentrations, suggesting that Hg exposure may lead to potentially negative effects to blacktip liver. In contrast, an evaluation of plasma levels for 14 heavy metals and 12 trace elements in white sharks, Carcharodon carcharias, did not find any negative effects of metal concentrations upon the determined shark health parameters, including total leukocytes, granulocyte to lymphocyte ratios, and shark body condition (Merly et al., 2019). Taken together, these studies suggest that the sublethal effects of metal concentrations on shark health are likely to depend on the species, life-stage, type and concentration of the accumulated metals, tissue type and associated physiological processes.

The present study evaluated the concentration levels of cobalt (Co), manganese (Mn), nickel (Ni), copper (Cu), iron (Fe), and mercury (Hg) in four tissues (gill, muscle, liver and rectal gland) opportunistically sampled from coastal sharks in Brazil, and tested for potential relationships between metal bioaccumulation and general shark health and homeostatic balance metrics. The reason for choosing these elements is multifold. First, Hg is an important contaminant routinely detected in sharks worldwide, resulting in negative health effects to both sharks and humans through shark meat consumption. Ni, is traditionally considered non-essential and has been reported as toxic, although mounting evidence has indicated it may be essential to fish (Pyle and Couture, 2012). Although all other elements are essential (Co, Mn, Cu, Fe), high concentrations are being detected in many regions worldwide, probably due to climate change effects, which are more devastating in coastal areas (EC, 2021), leading to increasing leaching from substrate to the water column and subsequent alterations in metal bioavailability (Machado et al., 2016). Furthermore, all the determined essential metals contribute to homeostasis in most vertebrates, as an integral part of proteins and enzymes. However, even essential elements might become potentially toxic when in concentrations above biological thresholds (Hauser-Davis and Lavradas, 2018).

To this end, four study hypotheses were empirically tested. First, that metals would show bioaccumulation in shark tissues, with concentrations increasing with shark size (Alves et al., 2016). Second, that among the four tested tissues, metal concentrations would be higher in the liver as organs containing lipid deposits tend to accumulate higher metal contents (Terrazas-López et al., 2016). Third, that overall shark health and homeostatic balance metrics would be impacted by high tissue concentrations of metals (Alves et al., 2016). Specifically, individuals with higher metal concentrations would exhibit evidence of decreased body condition and impaired osmoregulatory capacity, acid-base balance, metabolic energy, and liver functioning. Fourth and finally, we hypothesized that sex (Lopez et al., 2013) and life-stage (Frías-Espericueta et al., 2015) would influence differences in bioaccumulation patterns and their consequent effects upon systemic health (i.e., physical and nutritional condition).