Sublethal copper exposure induces respiratory stress in common
and gibel carp but not in rainbow trout
G. De Boeck
⁎
, K. Van der Ven, W. Meeus, R. Blust
Ecophysiology, Biochemistry and Toxicology Group, Department of Biology, University of Antwerp, Groenenborgerlaan 171, B-2020 Antwerp, Belgium
Received 1 August 2006; received in revised form 14 November 2006; accepted 14 November 2006
Available online 25 November 2006
Abstract
Rainbow trout, common carp, and gibel carp were exposed to sublethal Cu levels (1.0 or 1.7 μM) for 1 week. In rainbow trout, arterial oxygen
tension (P
aO
2
) remained normal and there was no indication of anaerobic metabolism. P
aO
2
was considerably lower in common and gibel carp and
Cu exposure decreased this further. The decrease was transient for common carp but persistent in gibel carp and coincided with an elevation in
arterial carbon dioxide tension (P
aCO
2
) indicating that all gas exchange was compromised in both cyprinid species. The disturbed gas exchange
resulted in acidosis, which was respiratory and metabolic for common carp but mainly respiratory for gibel carp. Gibel carp produced ethanol as
end product of their alternative anaerobic pathway. The hypothesis that hypertrophy and hyperplasia, resulting in increased diffusion distances, are
reducing P
aO
2
appeared invalid. Hypoventilation seems a more likely cause. Ionoregulatory parameters responded more uniform among species.
Fast and pronounced decreases in plasma sodium and chloride developed for all three species, independent of the observed gill damage. Rainbow
trout lost 20% of their plasma Na in the first 3 days, while common and gibel carp had only lost 13 and 16% respectively at that time. This
difference might be crucial when challenged with Cu exposure and allow a fish to survive the first shock phase and supports it the hypothesis that
sodium turnover is a key factor in predicting Cu toxicity.
© 2006 Elsevier Inc. All rights reserved.
Keywords: Blood gas; Aerobic and anaerobic metabolism; Ionoregulation; Gill damage; Oncorhynchus mykiss; Cyprinus carpio; Carassius auratus gibelio
1. Introduction
In salmonids, copper is believed to be a respiratory toxicant
only at high concentrations (Wilson and Taylor, 1993). At
elevated levels in freshwater it targets the gills, the main gas and
ion exchange surface in fish, causing mucous production, cell
swelling and epithelial lifting. These processes interfere with
respiration by increasing diffusion distance and ionoregulation by
inhibiting key transport processes (Mallat, 1985; Wood, 2001).
However, in cyprinids such as the common carp, effects on
respiration rates occur at relatively low copper concentrations (De
Boeck et al., 1995) despite the fact that this species is much more
resistant to Cu intoxication (De Boeck et al., 2004). In a
comparative study using rainbow trout, Oncorhynchus mykiss,
common carp, Cyprinus carpio, and gibel carp, Carassius
auratus gibelio, exposed to 1 μM of Cu, reductions in respiration
rates occurred for both common and gibel carp but not for rainbow
trout. Additionally, common carp showed clear indications of a
transient period of anaerobic metabolism resulting in an
acidification of its muscle tissue after 24 h of exposure (De
Boeck et al., 2006). For all three species swimming performance
measured as critical swimming speed was at least temporarily
reduced. The present study aimed to examine whether gas transfer
was compromised creating internal hypoxia in these species at
sublethal Cu levels, or whether gas transport is not restrained but
the cyprinid species display reduced energy consumption and
enter metabolic depression during Cu exposure. Gibel carp, a
close relative to the crucian carp, Carassius carassius, are well
equipped for metabolic depression (Nilsson and Renshaw, 2004)
and can switch to an alternative metabolic pathway producing
ethanol instead of lactate under hypoxic or anoxic conditions. As
lethal Cu levels differ considerably for the three species in this
study (De Boeck et al., 2004), we chose the exposure con-
centrations in the range of 1.0 to 1.7 μM, a sublethal concentration
for all species involved.
Comparative Biochemistry and Physiology, Part C 144 (2007) 380 – 390
www.elsevier.com/locate/cbpc
⁎
Corresponding author. Tel.: +32 3 2653348; fax: +32 3 2653497.
E-mail address: gudrun.deboeck@ua.ac.be (G. De Boeck).
1532-0456/$ - see front matter © 2006 Elsevier Inc. All rights reserved.
doi:10.1016/j.cbpc.2006.11.008