Aquatic Toxicology 142–143 (2013) 203–209
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Aquatic Toxicology
jou rn al hom ep age: www.elsevier.com/locate/aquatox
Copper interacts with nonylphenol to cancel the effect of nonylphenol
on fish chemosensory behaviour
Ashley J.W. Ward
a,∗
, Maria Thistle
b
, Khashayar Ghandi
c
, Suzanne Currie
b
a
School of Biological Sciences, University of Sydney, Sydney, NSW, Australia
b
Department of Biology, Mount Allison University, Sackville, NB, Canada
c
Department of Chemistry and Biochemistry, Mount Allison University, Sackville, NB, Canada
a r t i c l e i n f o
Article history:
Received 11 March 2013
Received in revised form 19 August 2013
Accepted 20 August 2013
Keywords:
Ecotoxicology
Shoaling
Sociality
Chemical ecology
Info-disruption
Social attraction
a b s t r a c t
The majority of ecotoxicological studies have been concerned with responses of organisms to a single
contaminant. While this approach remains valid, the challenge now is to understand the way in which
multiple contaminants and stressors interact to produce effects in study organisms. Here we take an
integrated biological and physico-chemical approach to understand the effects of 4-nonylphenol and
copper on fish (white perch, Morone americana) chemosensory behaviour. We show that a one hour
exposure to 2 g L
-1
nonylphenol removes chemosensory attraction to conspecific chemical cues, while
exposure to 5 g L
-1
copper for one hour had no significant effect on the fish’s attraction to these cues.
Further, we show that simultaneous exposure to both contaminants at the stated dosage and for the same
duration has no significant effect on the chemosensory attraction of white perch to conspecific chemical
cues suggesting that copper mediates the effect of nonylphenol on fish in this respect. Physico-chemical
data show that copper ions bind to nonylphenol in water, providing a mechanistic explanation for this
change in the effect of nonylphenol. Furthermore, the finding that the copper ions bind to the lone pair of
O on the nonylphenol molecule offers the tantalising possibility that it is this region of the nonylphenol
molecule that plays the key role in disrupting fish chemical communication.
© 2013 Elsevier B.V. All rights reserved.
1. Introduction
Pollution as a result of human activity presents a range of chal-
lenges for the organisms that live in those habitats. The effects
of such pollution may sometimes be acute and dramatic, such
as the mass deaths that occur periodically in response to major
chemical spills. But while these events capture headlines and atten-
tion, it is arguably the day-to-day and comparatively low-level
contamination of environments which present the greater long
term ecological challenge. Ecotoxicological studies have reported
a broad range of behavioural, physiological and cellular effects of
pollutants on aquatic organisms (Berrill et al., 1993; Little et al.,
1990; Sloman and Wilson, 2006).
The overwhelming majority of laboratory based ecotoxicology
studies have concentrated on the response of organisms to a single
chemical at one time. Although it is clearly necessary to understand
organismal responses to specific chemicals, a criticism that is some-
times made of this approach is that it fails to capture the complex
chemical situation encountered by animals in the wild, where many
contaminants may be present simultaneously (Cleveland et al.,
∗
Corresponding author. Tel.: +61 2 9351 4778; fax: +61 2 9351 4778.
E-mail address: ashley.ward@sydney.edu.au (A.J.W. Ward).
1986). Furthermore, there is sometimes a disparity between lab-
oratory and field studies of chemical ecology and ecotoxicology
whereby the findings of the latter fail to match the predictions of
the former (Archard et al., 2008; Grue et al., 2002; Marentette et al.,
2012). This may be because wild populations gradually acclimatize
to contaminated habitats, or that the effects of contaminants are
exaggerated in the potentially more stressful environment of the
laboratory (Marentette et al., 2012). Alternatively it may be because
multiple contaminants interact in the field to form chemical com-
plexes that change considerably the toxicological impact that each
chemical might produce on an organism in isolation. Specifically,
interacting chemicals could conceivably produce either synergistic,
additive or antagonistic effects on organisms (An et al., 2004; Wu
et al., 2013).
Contamination of aquatic habitats through the input of anthro-
pogenic chemicals is a widespread problem and the effects on
aquatic organisms are diverse (Harmon, 2009). One particular
problem that has been identified in recent years is the propen-
sity of contaminants, even at very low concentrations, to act as
‘info-disruptors’, impairing the chemosensory abilities of aquatic
organisms (Lurling and Scheffer, 2007). In fishes, chemical commu-
nication supports a suite of social behaviours, including shoaling,
territoriality and mate choice (Liley, 1982). Each individual fish
has a ‘chemical signature’ that is extremely important for social
0166-445X/$ – see front matter © 2013 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.aquatox.2013.08.010