Please cite this article in press as: Di Poi, C., et al., Cryptic and biochemical responses of young cuttlefish Sepia officinalis exposed to environmentally
relevant concentrations of fluoxetine. Aquat. Toxicol. (2014), http://dx.doi.org/10.1016/j.aquatox.2013.12.026
ARTICLE IN PRESS
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AQTOX-3721; No. of Pages 10
Aquatic Toxicology xxx (2014) xxx–xxx
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Aquatic Toxicology
jou rn al hom ep age: www.elsevier.com/locate/aquatox
Cryptic and biochemical responses of young cuttlefish Sepia officinalis
exposed to environmentally relevant concentrations of fluoxetine
Carole Di Poi
a,b
, Flavie Bidel
a,b
, Ludovic Dickel
a,b
, Cécile Bellanger
a,b,∗
a
Universit´ e de Caen Basse-Normandie, France
b
Groupe M´ emoire et Plasticit´ e comportementale, EA 4259, F-14032 Caen cedex, France
a r t i c l e i n f o
Article history:
Received 31 August 2013
Received in revised form
22 December 2013
Accepted 24 December 2013
Keywords:
Cephalopods
Selective Serotonin Reuptake Inhibitors
(SSRI)
Fluoxetine
Camouflage
Locomotor activity
Sand digging behavior
Monoamines
a b s t r a c t
Antidepressants released in the environment have the potential to generate neural disrupting effects
in non-target organisms, yet their putative effects on behaviors have never been studied in cephalopod
molluscs. This study assessed the impact of the antidepressant fluoxetine (FLX) on the efficiency of cryptic
behaviors (body patterns on uniform, checkerboard and sandy substrates), locomotor activity, and brain
chemistry in young cuttlefish exposed to environmental concentrations (1 and 100 ng L
-1
of FLX) dur-
ing the perinatal period. Behavioral responses of cuttlefish were monitored at hatching and two weeks
later, and brain monoamine contents were quantified at one month of age. FLX significantly altered the
camouflage efficiencies on uniform and sandy backgrounds only at the lowest concentration, but not
at 100 ng L
-1
. Hatchlings exposed to 1 ng L
-1
of FLX exhibited a duration exposure-dependent decrease
in the uniform camouflage. They also showed a significant increase of the frequency of sand digging
behaviors which might make them highly visible to predators in nature. When tested again two weeks
later, cuttlefish seemed to have recovered and no more behavioral alterations were observed showing
a transitory effect of the antidepressant. FLX did not affect the levels of serotonin, norepinephrine and
their metabolites; however, it seemed to influence dopaminergic activity between the two FLX-exposed
groups. The results show for the time that environmentally realistic concentrations of a single SSRI sig-
nificantly impair the cryptic performances of newly hatched cuttlefish, and may ultimately reduce their
chance for survival.
© 2014 Elsevier B.V. All rights reserved.
1. Introduction
The coleoid cephalopods (octopuses, cuttlefishes and squids)
display unique defensive behaviors controlled by one of the
most sophisticated nervous system within invertebrates (Nixon
and Young, 2003; Dickel et al., 2013). They express two major
antipredator strategies (reviewed in Hanlon and Messenger, 1996).
The first one, called primary defense, serves to reduce the chance
of being detected by a potential predator using cryptic behaviors.
Cephalopods can rapidly change color and exhibit different body
patterns. According to Hanlon and Messenger (1988), the cuttle-
fish Sepia officinalis can adopt three main types of body patterns for
camouflage when settled on the bottom: “uniform/stipple”, “mot-
tle” and “disruptive” that can be regarded as mosaics varying in
color, shape, size, intensity and texture. Uniform patterns are usu-
ally displayed on uniform backgrounds, whereas cuttlefish exhibit
∗
Corresponding author at: Universit ´ e de Caen Basse-Normandie, France.
Tel.: +33 231 566 879.
E-mail addresses: carole.dipoi@gmail.com (C. Di Poi), favie.bidel@unicaen.fr
(F. Bidel), ludovic.dickel@unicaen.fr (L. Dickel), cecile.bellanger@unicaen.fr
(C. Bellanger).
more complex patterns such as mottle pattern on sandy bottoms or
disruptive pattern on contrasted substrates containing gravel, peb-
bles or shells. This extraordinary ability is due to the presence of
chromatophores on their skin; i.e. neuromuscular organs controlled
by optic lobes in the brain involved in the integration of visual infor-
mation that serve on body patterning (Messenger, 2001). Among
other cryptic behaviors, the cuttlefish can bury in sand to avoid
potential predators (Mather, 1986; Boletzky, 1987). In the genus
Sepia, digging is a relatively short and fixed behavioral sequence
lasting less than 5 s on fine sand (Mather, 1986). Secondary defenses
are used when the cuttlefish has already been detected by a preda-
tor. Threat displays include flight response frequently accompanied
with ink ejection, as well as deimatic behavior characterized by
the appearance of black eyespots on the dorsal mantle of the ani-
mal (reviewed in Hanlon and Messenger, 1996). Cuttlefish are able
to exhibit all these complex behaviors from hatching; although
their expression needs adjusting and improves with development
and learning from their environment (Poirier et al., 2004, 2005).
A recent study shows that xenobiotic pollutants discharged in the
marine environment can impact cognitive abilities of young cut-
tlefish and may ultimately modify these basic behaviors (Di Poi
et al., 2013). We showed that chronic exposures to environmentally
relevant concentrations of the antidepressant fluoxetine impair
0166-445X/$ – see front matter © 2014 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.aquatox.2013.12.026