Abstract
Marine bivalves are frequently exposed to multiple co-occurring challenges such as temperature extremes and anthropogenic pollution. These stressors can elicit negative effects on several biological pathways, including antioxidant and neuroendocrine-immune (NEI) systems, leading to immune disorders and altered immunocytes functionality. Since interactive mechanisms of action and resulting outcomes are still scarcely explored, we examined the single and combined effects of increased temperature (+5°C) and cadmium (20 μg/L) in the Mediterranean mussel Mytilus galloprovincialis. Analyzed parameters included cholinergic system in gills and hemolymph (acetylcholinesterase activity, AChE), total oxyradical scavenging capacity in gills and key functional processes in hemocytes, including lysosomal membrane stability, hemocytes subpopulations ratio, phagocytosis capacity, and onset of genotoxic damage. Results highlighted interactive inhibition of AChE activity along to a concomitant increased total oxyradical scavenging capacity, confirming neuroendocrine-immune system (NEI) disturbance and oxidative pressure. In hemocytes, lysosomal membrane stability and granulocytes:hyalinocytes ratio revealed additive effects of stressors, while a consistent reduction of phagocytosis was caused by temperature stress, with a slightly antagonistic effect of cadmium. Pearson’s correlation statistics provided either positive or negative relationships between investigated parameters and stressors, allowing to hypothesize putative mechanism of immune system functional alterations. The overall results suggest that the occurrence of short-term events of increased temperature and concomitant metal exposure could elicit interactive and negative effects on immune system efficiency of marine organisms.
Highlights
Marine bivalves living in coastal areas are currently subjected to multiple co-occurring stressors: organisms are exposed, among others, to relevant loads of inorganic pollutants deriving from landbased human activities and frequent events of thermal stress caused by ongoing ocean warming and increasing intensity of marine heatwaves (Oliver et al, 2018, 2019; IPCC, 2019)
Thermal stress condition (25◦C) was chosen to simulate a short-term heatwave scenario based on past events of marine heatwaves in the Mediterranean sea,1 2 while cadmium concentration was based on environmentally realistic scenarios of polluted coastal areas (Neff, 2002; Beiras et al, 2003; Martín-Díaz et al, 2005; AbdAllah and Moustafa, 2007; Süren et al, 2007)
Two-way analysis of variance revealed a significant modulation of temperature on phagocytosis rate (Figure 3B and Table 1, F = 92.27, p < 0.001) which was lowered in HS treated organisms either with or without Cd
Summary
Marine bivalves living in coastal areas are currently subjected to multiple co-occurring stressors: organisms are exposed, among others, to relevant loads of inorganic pollutants deriving from landbased human activities (e.g., trace metals, EEA, 2019; Bates et al, 2021) and frequent events of thermal stress caused by ongoing ocean warming and increasing intensity of marine heatwaves (Oliver et al, 2018, 2019; IPCC, 2019). Current knowledge on the interactions between thermal stress and trace metals on marine ectotherms biology suggests additive or synergic mechanisms, with thermal stress enhancing deleterious effects of metals and vice versa: temperature can trigger metal uptake through increased metabolism and membranes permeability, while, trace metals can impair oxygen metabolism and affect thermal tolerance (Lannig et al, 2008; Sokolova and Lannig, 2008; Lan et al, 2020) Both trace metals and thermal stress are known to disrupt bivalves optimal physiological functioning through the inhibition of defense mechanisms, as the capability to counteract onset of oxidative conditions and to maintain the functionality of immune system. When oxidative pressure is not properly counteracted by the antioxidants network, the onset of oxidative damages to lipids, proteins, and DNA is observed in tissues of marine organisms (Izagirre et al, 2014; Múgica et al, 2015; Coppola et al, 2017)
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