Does dissolved organic carbon from Amazon black water (Brazil) help a native species, the tambaqui Colossoma macropomum to maintain ionic homeostasis in acidic water?

Abstract

To assess how the quality and properties of the natural dissolved organic carbon (DOC) could drive different effects on gill physiology, we analysed the ionoregulatory responses of a native Amazonian fish species, the tambaqui Colossoma macropomum, to the presence of dissolved organic carbon (DOC; 10 mg l−1) at both pH 7.0 and pH 4.0 in ion‐poor water. The DOC was isolated from black water from São Gabriel da Cachoeira (SGC) in the upper Rio Negro of the Amazon (Brazil) that earlier been shown to protect a non‐native species, zebrafish Danio rerio against low pH under similar conditions. Transepithelial potential (TEP), net flux rates of Na+, Cl− and ammonia and their concentrations in plasma and Na+, K+ ATPase; v‐type H+ ATPase and carbonic anhydrase activities in gills were measured. The presence of DOC had negligible effects at pH 7.0 apart from lowering the TEP, but it prevented the depolarization of TEP that occurred at pH 4.0 in the absence of DOC. However, contrary to our initial hypothesis, SGC DOC was not protective against the effects of low pH. Colossoma macropomum exposed to SGC DOC at pH 4.0 experienced greater net Na+ and Cl− losses, decreases of Na+ and Cl− concentrations in plasma and elevated plasma ammonia levels and excretion rates, relative to those exposed in the absence of DOC. Species‐specific differences and changes in DOC properties during storage are discussed as possible factors influencing the effectiveness of SGC DOC in ameliorating the effects of the acid exposure.

The physiology of fish in acidic waters rich in dissolved organic carbon, with specific reference to the Amazon basin: Ionoregulation, acid–base regulation, ammonia excretion, and metal toxicity

“…Consistent with previously described TEP results in salmonids at low pH (McWilliams & Potts, 1978; Ye et al, 1991), exposure of tambaqui to low pH caused depolarization (Sadauskas‐Henrique et al, 2019; Wood et al, 1998). However, exposure to DOC from SGC at circumneutral pH caused hyperpolarization, and the DOC completely mitigated the depolarization of TEP at low pH (Sadauskas‐Henrique et al, 2019). This occurred despite the inability of this DOC to protect against net ion loss at low pH, perhaps because it had degraded during storage, as discussed earlier.…”

“…While both low pH and DOC individually alter TEP, DOC may offer protection over changes in the electrical properties of the gill in response to low pH. Consistent with previously described TEP results in salmonids at low pH (McWilliams & Potts, 1978; Ye et al, 1991), exposure of tambaqui to low pH caused depolarization (Sadauskas‐Henrique et al, 2019; Wood et al, 1998). However, exposure to DOC from SGC at circumneutral pH caused hyperpolarization, and the DOC completely mitigated the depolarization of TEP at low pH (Sadauskas‐Henrique et al, 2019).…”

“…However, after 2 years of refrigerator storage, it had lost about half of its color as indicated by the decline in SAC 340 , and the mean MW had also declined, though the relative distribution (quantified by PARAFAC) of humic acid‐, fulvic acid‐, and amino acid‐like components remained unchanged. When tested at this time, SGC DOC exacerbated rather than protected against ionoregulatory disturbance in a native species, the tambaqui, even though it still exerted hyperpolarizing effects on TEP (Sadauskas‐Henrique et al, 2019). Unfortunately, species differences and the potential degradation of the DOC confounded interpretation in that investigation.…”

“…Therefore, knowledge of fish gill electrophysiology is essential in the interpretation of ion movement across the gills, as has become apparent from recent studies on salt toxicity (Po & Wood, 2021; Wood et al, 2020). DOC, much like other water quality parameters (e.g., hardness, pH and salinity; Potts, 1984) may have a large impact on the electrical properties of the gill (Galvez et al, 2008; Sadauskas‐Henrique et al, 2019).…”

“…The effects of fluctuations in other water quality parameters (e.g., pH, alkalinity, Ca, Na, salinity) on gill function have been extensively studied by physiologists but the effects of DOC on the ion transporting properties of the gill remain relatively unexplored. DOC is a critically important water quality parameter to consider for ecological understanding and risk assessment as it may have comparable or greater effects on freshwater fish physiology (e.g., ionoregulation, acid–base balance, and acute metal toxicity) than the previously mentioned and well‐studied water quality parameters (Duarte et al, 2016; Gonzalez et al, 2002; Sadauskas‐Henrique et al, 2019; Wood et al, 2011; Wood et al, 2003, 1998).…”