Content uploaded by Joanna Pijanowska
Author content
All content in this area was uploaded by Joanna Pijanowska on Jan 21, 2016
Content may be subject to copyright.
BIOLOGY OF CLADOCERA
Role of melatonin in the control of depth distribution
of Daphnia magna
Piotr Bentkowski
•
Magdalena Markowska
•
Joanna Pijanowska
Published online: 7 March 2010
Ó Springer Science+Business Media B.V. 2010
Abstract Previous studies confirmed the presence
of melatonin in Daphnia magna and demonstrated
diurnal fluctuations in its concentration. It is also
known that in several invertebrate species, melatonin
affects locomotor activity. We tested the hypothesis
that this hormone is involved in the regulation of
Daphnia diel vertical migration (DVM) behaviour
that is well recognized as the adaptive response to
predation threat. Using ‘plankton organs’, we studied
the effect of three concentrations of exogenous
melatonin (10
-5
,10
-7
,10
-9
M) on DVM of both
female and male D. magna in the presence or absence
of chemical cue (kairomone) of planktivorous fish.
Depth distribution was measured six times a day,
using infrared-sensitive closed circuit television cam-
eras. Our results showed a significant effect of
melatonin on the mean depth of experimental popu-
lations, both males and females, but only when
melatonin was combined with fish kairomone.
Females stayed, on average, closer to the surface than
males, both responding to the presence of kairomone
by descending to deeper strata. In the presence of
exogenous melatonin and with the threat of predation,
Daphnia stayed closer to the surface and their
distribution was more variable than that of individu-
als, which were exposed to the kairomone alone.
Approaching the surface in the presence of predation
threat seems to be maladaptive. We postulate the role
of melatonin as a stress signal inhibitor in molecular
pathways of response to predation threat in Cladocera.
Keywords Daphnia Depth distribution
Melatonin Predation
Introduction
The presence of melatonin has been reported in many
organisms, including bacteria (Tilden et al., 1997a),
unicellular algae (Balzer & Hardeland, 1991), higher
plants (Reiter & Tan, 2002), invertebrates (Vivien-
Roels & Pe
´
vet, 1993), and vertebrates (Gern et al.,
Guest editors: M. Silva-Briano & S. S. S. Sarma / Biology of
Cladocera (Crustacea): Proceedings of the VIII International
Cladocera Symposium
P. Bentkowski J. Pijanowska
Faculty of Biology, Department of Hydrobiology,
University of Warsaw, Banacha 2,
02-097 Warsaw, Poland
J. Pijanowska
e-mail: j.e.pijanowska@uw.edu.pl
M. Markowska
Faculty of Biology, Department of Animal Physiology,
University of Warsaw, Miecznikowa 1,
02-096 Warsaw, Poland
e-mail: markosia@biol.uw.edu.pl
P. Bentkowski (&)
School of Environmental Sciences,
University of East Anglia, Norwich NR4 7TJ, UK
e-mail: P.Bentkowski@uea.ac.uk
123
Hydrobiologia (2010) 643:43–50
DOI 10.1007/s10750-010-0134-x
1986). It functions in free radical scavenging, the
regulation of body mass and energetic metabolism,
and is a key component of the biological clock
responsible for modulating physiological rhythms
(for reviews see Hardeland & Poeggeler, 2003;
Pandi-Perumal et al., 2006). With regard to the
effects of melatonin in invertebrates, it has been
shown that application of this hormone can alter
locomotory activity in the cricket Acheta domesticus
(Yamano et al., 2001) and the crayfish Procambarus
clarkii (Tilden et al., 2003); it can influence regen-
eration processes in the planarian Dugesia japonica
(Yoshizawa et al., 1991), the nemertean Lineus
lacteus (Arnoult & Vernet, 1995) and the crab Uca
pugilator (Tilden et al., 1997b); and it can alter life
history and reproduction in the aphid Acyrthosiphon
pisum (Gao & Hardie, 1997) and the dinoflagellate
Gonyaulax polyedra (Balzer & Hardeland, 1991).
In an earlier study, we found that melatonin is
present in the cladoceran Daphnia magna, being
located mainly in the optic nerves and ganglia as well
as in thoracopodes. It exhibits a diurnal rhythm, with
the peak abundance occurring during the light hours
(Markowska et al., 2009). Kashian & Dodson (2004)
detected no effect of melatonin application on either
the growth rate or reproduction of Daphnia.
Zooplankton diel vertical migration (DVM) as an
anti-predator strategy has been observed in a number of
prey–predator interactions (e.g. Bollens & Frost, 1989;
Dawidowicz et al., 1990; Neill, 1990; Dawidowicz,
1993; Loose, 1993). In Daphnia, migratory behaviour
is induced by the chemical cues (kairomones) released
to water by planktivorous fish (Dawidowicz & Loose,
1992a). The most typical pattern of DVM is searching
the dark refuge against visual predation in the deep
strata during the day and approaching the surface at
night, to exploit the epilimnetic resources. Reduced
growth and reproduction rates in low temperatures of
deeper water are well-documented costs of avoiding
the risk of being eaten (Dawidowicz & Loose, 1992a).
Though ecological significance of DVM has been well
recognized (e.g. Ringelberg, 1999), the understanding
of its physiological and biochemical mechanisms is
still poor.
As melatonin is known to alter locomotory activity
depending on light conditions, we tested the hypoth-
esis that it is involved in the regulation of the
phenomenon of DVM in Daphnia, the onset and
offset of which are triggered by light.
Materials and methods
Daphnia magna
clone P3 originating from Binnen-
see, a shallow brackish lake in North Germany
inhabited by fish (Lampert, 1991), was used in the
experiment. Animals were obtained from the third
or later clutches of a synchronized population of
mothers, originating from a single female. Mothers
were kept at a temperature of 22 ± 2°C, under a long
day photoperiod (16L:8D), at a density of 10 ind. l
-1
in water from a shallow, eutrophic lake near Warsaw,
that had been stored and aerated for several weeks
and then filtrated through a glass fibre filter (GF/C,
Sartorius) prior to use. They were fed the algae
Scenedesmus obliquus at a concentration of
1mgC
org
l
-1
. Algae were grown in xenic (contain-
ing bacteria) batch cultures on Z/4 medium, under
continuous illumination from white fluorescent
lamps, at 21 ± 1°C.
The experiment was conducted in a ‘plankton
organ’: an apparatus described by Dawidowicz &
Loose (1992a). Glass flow-through tubes (60 cm
long, 1.5 cm in diameter) were arranged vertically in
an aquarium (60 cm 9 100 cm 9 15 cm) located
in an air-conditioned darkroom. Medium (same as in
mothers’ culture) was delivered individually to each
tube using a peristaltic pump (Ismatec). Thermal
stratification in the tubes (21 ± 1°C at the surface
and 10 ± 0.5°C at the bottom) was achieved by
heating the surface waters in the aquarium and
cooling the bottom. Experimental animals (neonates
born within the previous 8 h) were transferred to
eight tubes, at three individuals per tube. Altogether,
eight treatments were applied by making additions to
the media in the separate tubes:
1 One control (i.e. medium without additions)
2–4 Three different melatonin concentrations
(10
-5
,10
-7
,10
-9
M)
5 Fish kairomone
6–8 Fish kairomone plus three different melatonin
concentrations (10
-5
,10
-7
,10
-9
M).
The fish kairomone used was an extract of the
faeces of Leucaspius delineatus (Cyprynidae) fed
with live D. magna, prepared according to the
procedure of Slusarczyk & Rygielska (2004) and
stored frozen (-20°C) before use. The concentration
of kairomone was equivalent to the presence of one
fish in 10 l of water. Melatonin (Sigma) was
44 Hydrobiologia (2010) 643:43–50
123
dissolved in acetone (0.1% solution) and stored in a
refrigerator (4°C). The same acetone concentration
was in treatment 1 and 5. Earlier studies have shown
that low concentrations of acetone do not influence
Daphnia and can be used as a melatonin solvent
(Kashian & Dodson, 2004). The media in the tubes
were changed twice a day: after the laboratory sunrise
and before the laboratory sunset.
During daytime, the system was illuminated from
above by four halogen bulbs (20 W, 12 V, Phillips)
shining through a frosted plexiglass screen to provide
homogeneous diffused light. Apart from the front
panel, the sides of the aquarium were covered with
black paper. Two monochromatic closed circuit
television (CCTV) cameras were installed in front
of the aquarium and focused on the upper and lower
parts of the tubes, respectively. The cameras were
connected to a PC, which recorded 1-min long videos
at 4, 8 and 12 h after light-on (day), and 2, 4 and 6 h
after light-off (night). At night, the visible light was
turned off and the system was illuminated by 100
infra red light emitting diodes (TSAL-6400, peak
wavelength 940 nm), only when video recordings
were made. The diodes were placed inside the
aquarium in two rows (50 in each) in two plexiglass
tubes, positioned behind the flow-through tubes
containing Daphnia (Fig. 1). The first video was
recorded in the morning on the first day of the
experiment and recording was continued over the
next 5 days. After the completion of the experiment,
the position of individual Daphnia in each tube was
recorded at each time point (with 0.5 cm accuracy)
while viewing the video. Depth of each animal was
determined in the very first moment when it appeared
on the screen. For analysis, video tapes from different
treatments were randomly selected.
The resolution of the CCTV images limited the
number of tubes that could be examined simulta-
neously to 8 (i.e. each of the separate treatments
without replicates). The whole experiment was per-
formed three times with female Daphnia, but only
once with males.
For analysis of the depth distribution of female
Daphnia, five-way independent ANOVA was applied
(SPSS Statistics 16.0), with day, hour, the presence or
absence of kairomone, melatonin concentration and
replicate/experiment as independent variables. As the
experiment was run only once for males, four-way
independent ANOVA was used to statistically analyze
their depth distribution.
Results
Daphnia exposed to the chemical trace of fish
presence stayed deeper in the water than those kept
free of kairomone. Furthermore, the former animals
performed DVMs, approaching the surface during the
night and descending towards the bottom during the
day, although the difference between control and
kairomone treatment was less pronounced in males
than in females (Fig. 2). However, the differences in
behaviour due to the threat of predation became
clearly visible after 48 h of exposure, with the mean
depth of Daphnia females differing significantly
between the first 2 days and the remaining part of
the experiment, so that two homogeneous groups
could be differentiated with a Tukey HSD post hoc
test. These results are consistent with earlier research
showing that smaller (i.e. younger) Daphnia are less
vulnerable to fish predation and prefer surface waters,
also during the daytime (Hansson & Hylander, 2009).
Fig. 1 Experimental setup
of the ‘plankton organ’ used
to examine the effects of
melatonin and threat of
predation (fish kairomone)
on the depth distribution of
Daphnia. The position of
the infra red light emitting
diodes (IR LED) used for
illumination during
nocturnal video recording is
shown. Aquarium
dimensions are
60 cm 9 100 cm 9 15 cm
Hydrobiologia (2010) 643:43–50 45
123
In males, three separate homogeneous groups were
differentiated: on day 1, day 3 and days 2, 4, 5
(Tukey HSD post hoc test). Therefore, data collected
after the first 48 h of the experiment were selected for
further analysis. Since then, the mean day depth of
females in the presence of kairomone averaged
32.2 ± 2.5 vs. 3.3 ± 0.5 cm in the control treatment,
whereas in males it was 38.7 ± 1.7 vs. 14.9 ±
3.2 cm (mean ± SE).
In females, the presence of kairomone, melatonin
concentration, light conditions, day and hour of the
experiment had significant effects on Daphnia depth
selection, and all interactions of these main effects
were also significant (Table 1). In the absence of fish
kairomone, all animals stayed close to the water’s
surface in all treatments, regardless of the melatonin
concentration (Fig. 3A). However, a clear effect of
melatonin on Daphnia depth distribution was
observed in the presence of fish kairomone: Daphnia
exposed to melatonin tended to stay on average
12 cm closer to the surface (their mean day depth was
20 ± 1.4 vs. 32.2 ± 2.5 cm in the presence of
kairomone alone) and their distribution was highly
variable (Fig. 3B). A highly significant interaction
between the concentration of melatonin and the
presence of kairomone was identified (Table 1).
A significant difference was only observed between
the highest concentration of melatonin and no
exogenous melatonin in the medium (Table 2).
We also observed significant effects of all main
factors on the mean depth of Daphnia males (Table 3).
All interactions were significant with the exception of
that between melatonin concentration and hour
(Table 3). Males stayed close to the surface (albeit
deeper than females) in the absence of kairomone,
regardless of the melatonin concentration (Fig. 4A). In
the presence of the chemical trace of fish, melatonin
had a significant effect on male depth selection
(Fig. 4B), their mean day depth averaging 24.2 ±
1.6 vs. 38.7 ± 1.7 cm in the presence of kairomone
alone and the strength of its impact depending on the
concentration of the hormone. The lowest melatonin
concentration caused the strongest effect, forcing
males to approach the surface (Table 4).
Discussion
Our results clearly indicate that depth distribution of
D. magna can be influenced by melatonin. To our
knowledge, this is the first evidence that exogenous
melatonin can affect Daphnia migratory behaviour.
In the presence of fish kairomone, melatonin
appeared to ‘push’ animals closer to the surface.
This influence was observed only when the applied
melatonin was accompanied by the threat of preda-
tion, suggesting the involvement of this hormone in
the response to stress. This function of melatonin has
also been proposed in vertebrates. In several studies,
it has been observed that melatonin counteracts the
effects of stress (Reiter et al., 2000, 2008; Bob &
Fedor-Freybergh, 2008
).
Constant residing in surface layers brings fitness
advantages, since high food availability and high
temperature enable faster growth and reproduction as
Fig. 2 Depth distribution (mean ± SEM) of Daphnia females
(A) and males (B) in the presence and absence of fish
kairomone. Grey bars indicate night hours
46 Hydrobiologia (2010) 643:43–50
123
compared with deeper layers of water column, less
profitable in terms of temperature and food conditions
(Guisande et al., 1991; Dawidowicz & Loose, 1992a).
The animals not exposed to fish kairomone stayed,
indeed, close to the surface. When planktivorous
visually hunting fish are present, the risk of being
eaten during the day surpass potential benefits, unless
Daphnia are small enough not to become vulnerable
(Hansson & Hylander, 2009). Since metabolic costs
of up and down swimming are negligible in Daphnia
(Dawidowicz & Loose, 1992b), the optimal strategy
to overcome this trade-off is to descend deeper during
the day, to seek for a dark refuge against visually
hunting fish and to exploit the resources of surface
water during the night time. Approaching closer to
the surface under predation threat by melatonin-
treated animals seems to be maladaptive since it
exposes Daphnia to an increased risk from the fish. It
has recently been shown that melatonin is able to
reduce the expression of Hsp 40, Hsp 70 and Hsp 90
genes elevated after stress treatment (adriamycin,
lipopolysaccharide or arsenite) in several cell culture
systems (Catala
´
et al., 2007; Esposito et al., 2008;
Lin et al., 2008). Changes in the expression of heat
shock proteins (Hsp 60, Hsp 70, Hsp 40) are a
potential marker of kairomone-induced predator
Table 1 Effects of
different factors on depth
distribution of Daphnia
females (main effect and
interactions, five-way
independent ANOVA)
Factor df FP
Day 4 52.488 \0.0005
Hour 5 14.504 \0.0005
Kairomone 1 2149.0 \0.0005
Melatonin 3 4.972 0.002
Replicate 2 458.209 \0.0005
Day 9 hour 20 5.939 \0.0005
Day 9 kairomone 4 85.711 \0.0005
Day 9 melatonin 12 5.423 \0.0005
Day 9 replicate 8 24.487 \0.0005
Hour 9 kairomone 5 3.854 0.002
Hour 9 melatonin 15 4.278 \0.0005
Hour 9 replicate 10 18.815 \0.0005
Kairomone 9 melatonin 3 18.558 \0.0005
Kairomone 9 replicate 2 137.921 \0.0005
Melatonin 9 replicate 6 19.575 \0.0005
Day 9 hour 9 kairomone 20 5.335 \0.0005
Day 9 hour 9 melatonin 60 1.692 0.001
Day 9 hour 9 replicate 39 6.667 \0.0005
Day 9 kairomone 9 melatonin 12 2.789 0.001
Day 9 kairomone 9 replicate 8 25.750 \0.0005
Day 9 melatonin 9 replicate 24 3.201 \0.0005
Hour 9 kairomone 9 melatonin 15 3.065 \0.0005
Hour 9 kairomone 9 replicate 10 10.528 \0.0005
Hour 9 melatonin 9 replicate 30 2.552 \0.0005
Kairomone 9 melatonin 9 replicate 6 16.187 \0.0005
Day 9 hour 9 kairomone 9 melatonin 60 1.663 0.001
Day 9 hour 9 kairomone 9 replicate 39 5.909 \0.0005
Day 9 hour 9 melatonin 9 replicate 117 1.864 \0.0005
Day 9 kairomone 9 melatonin 9 replicate 24 5.594 \0.0005
Hour 9 kairomone 9 melatonin 9 replicate 30 2.942 \0.0005
Day 9 hour 9 kairomone 9 melatonin 9 replicate 111 1.959 \0.0005
Hydrobiologia (2010) 643:43–50 47
123
stress (Pijanowska & Kloc, 2004; Pauwels et al.,
2005). It may be, therefore, postulated that one of the
mechanisms responsible for the effect of exogenous
melatonin on Daphnia depth selection involves
reduction of kairomone-induced Hsp expression and
thus, reversal of the physiological effect of kairo-
mone action.
The effect of melatonin on Daphnia appeared
more pronounced during the day than at night. In
female Daphnia there was no linear correlation
between the exogenous melatonin concentration and
the strength of the response to its presence. In males,
however, the lowest melatonin concentration pro-
duced the most visible effect, with animals in this
treatment group migrating closest to the surface.
Previously, we demonstrated that melatonin levels in
Daphnia are highest in the middle of the light phase
(Markowska et al., 2009). Therefore, it is possible
that sensitivity to melatonin is also higher during the
day. As Daphnia produces melatonin in a rhythmical
manner and, simultaneously, its diurnal behaviour is
influenced by exogenous melatonin, it may be
speculated that this hormone plays a role in the
regulation of a light-triggered response to predation
in cladocerans.
As we do not know how much of the hormone is
absorbed by these animals from the medium or the
resultant ratio between endo- and exogenous levels of
melatonin, any attempt to explain this phenomenon
remains highly speculative at this stage. Further
Fig. 3 Effect of different melatonin concentrations on depth
distribution (mean ± SEM) of Daphnia females in the absence
(A) and presence of fish kairomone (B). Grey bars indicate
night hours
Table 2 Comparison of the impact of different melatonin
concentrations on depth distribution of Daphnia females
(Tukey HSD post hoc test, P = 0.05)
Melatonin
concentration
N Mean depth (cm)
Subset 1 Subset 2
0 M 471 17.293
10
-9
M 514 16.011 16.011
10
-7
M 499 16.665 16.665
10
-5
M 504 15.860
P 0.438 0.073
Table 3 Effects of different factors on depth distribution of
Daphnia males (main effect and interactions, four-way independent
ANOVA)
Factor df FP
Day 4 55.739 \0.0005
Hour 5 21.230 \0.0005
Kairomone 1 383.835 \0.0005
Melatonin 3 49.439 \0.0005
Day 9 hour 20 4.539 \0.0005
Day 9 kairomone 4 17.387 \0.0005
Day 9 melatonin 12 6.542 \0.0005
Hour 9 kairomone 4 5.989 \0.0005
Hour 9 melatonin 15 2.468 0.002
Kairomone 9 melatonin 3 5.916 0.001
Day 9 hour 9 kairomone 20 2.507 \0.0005
Day 9 hour 9 melatonin 60 1.911 \0.0005
Day 9 kairomone 9 melatonin 12 10.262 \0.0005
Hour 9 kairomone 9 melatonin 15 2.251 0.005
Day 9 hour 9 kairomone 9 melatonin 42 2.142 \0.0005
48 Hydrobiologia (2010) 643:43–50
123
investigations are necessary to identify the direct
pathways (including molecular) by which melatonin
affects Daphnia behavioural responses to biotic stress.
Acknowledgements This research was supported by
Ministry of Science and Higher Education (Poland) grants 2
P04F 036 26 and N304 094135.
References
Arnoult, F. & G. Vernet, 1995. Inhibition of regeneration by
melatonin in nemertean worms of the genus Lineus.
Comparative Biochemistry and Physiology – Part A:
Physiology 110: 319–328.
Balzer, I. & R. Hardeland, 1991. Photoperiodism and effects of
indoleamines in a unicellular alga, Gonyaulax polyedra.
Science 253: 795–797.
Bob, P. & P. Fedor-Freybergh, 2008. Melatonin, conscious-
ness, and traumatic stress. Journal of Pineal Research 44:
341–347.
Bollens, S. & B. Frost, 1989. Predator-induced diet vertical
migration in a planktonic copepod. Journal of Plankton
Research 11: 1047–1065.
Catala
´
, A., A. Zvara, L. G. Puska
´
s & K. Kitajka, 2007.
Melatonin-induced gene expression changes and its pre-
ventive effects on adriamycin-induced lipid peroxidation
in rat liver. Journal of Pineal Research 42: 43–49.
Dawidowicz, P., 1993. Diel vertical migration in Chaoborus
flavicans: population patterns vs. individual tracks. Archiv
fu
¨
r Hydrobiologie–Beiheft Ergebnisse der Limnologie 39:
19–28.
Dawidowicz, P. & C. J. Loose, 1992a. Metabolic costs during
predator-induced diel vertical migration of Daphnia.
Limnology and Oceanography 37: 1589–1595.
Dawidowicz, P. & C. J. Loose, 1992b. Cost of swimming by
Daphnia during diel vertical migration. Limnology and
Oceanography 37: 665–669.
Dawidowicz, P., J. Pijanowska & K. Ciechomski, 1990.
Vertical migration of Chaoborus larvae is induced by the
presence of fish. Limnology and Oceanography 35: 1631–
1637.
Esposito, E., A. Iacono, C. Muia
`
, C. Crisafulli, G. Mattace
Raso, P. Bramanti, R. Meli & S. Cuzzocrea, 2008. Signal
transduction pathways involved in protective effects of
melatonin in C6 glioma cells. Journal of Pineal Research
44: 78–87.
Gao, N. & J. Hardie, 1997. Melatonin and the pea aphid,
Acyrthosiphon pisum. Journal of Insect Physiology 43:
615–620.
Gern, W. A., D. Duvall & J. M. Nervina, 1986. Melatonin: a
discussion of its evolution and actions in vertebrates.
American Zoologist 26: 985–996.
Guisande, C., A. Duncan & W. Lampert, 1991. Trade-offs in
Daphnia vertical migration strategies. Oecologia 87: 357–
359.
Hansson, L. & S. Hylander, 2009. Size-structured risk assess-
ments govern Daphnia migration. Proceedings of the
Royal Society B: Biological Sciences 276: 331–336.
Hardeland, R. & B. Poeggeler, 2003. Non-vertebrate melato-
nin. Journal of Pineal Research 34: 233–241.
Kashian, D. R. & S. I. Dodson, 2004. Effects of vertebrate hor-
mones on development and sex determination in Daphnia
magna. Environmental Toxicology and Chemistry 23:
1282–1288.
Fig. 4 Effect of different melatonin concentrations on depth
distribution (mean ± SEM) of Daphnia males in the absence
(A) and presence of fish kairomone (B). Grey bars indicate
night hours
Table 4 Comparison of the impact of different melatonin
concentrations on depth distribution of Daphnia males (post
hoc Tukey HSD test, P = 0.05)
Melatonin
concentration
N Mean depth (cm)
Subset 1 Subset 2 Subset 3 Subset 4
0 M 122 22.254
10
-9
M 179 15.159
10
-7
M 144 25.465
10
-5
M 156 17.949
P 1.000 1.000 1.000 1.000
Hydrobiologia (2010) 643:43–50 49
123
Lampert, W., 1991. The dynamics of Daphnia magna in a
shallow lake. Internationale Vereinigung fu
¨
r Theoretische
und Angewandte Limnologie 24: 795–798.
Lin, A. M., S. F. Feng, P. L. Chao & C. H. Yang, 2008.
Melatonin inhibits arsenite-induced peripheral neurotox-
icity. Journal of Pineal Research 46: 64–70.
Loose, C. J., 1993. Daphnia diel vertical migration behavior:
response to vertebrate predator abundance. Archiv fu
¨
r
Hydrobiologie–Beiheft Ergebnisse der Limnologie 39:
29–36.
Markowska, M., P. Bentkowski, M. Kloc & J. Pijanowska,
2009. Presence of melatonin in Daphnia magna. Journal
of Pineal Research 46: 242–244.
Neill, W. E., 1990. Induced vertical migration in copepods as a
defence against invertebrate predation. Nature 345: 524–
526.
Pandi-Perumal, S. R., V. Srinivasan, G. J. M. Maestroni, D. P.
Cardinali, B. Poeggeler & R. Hardeland, 2006. Melatonin:
nature’s most versatile biological signal? FEBS Journal
273: 2813–2838.
Pauwels, K., R. Stoks & L. de Meester, 2005. Coping with
predator stress: interclonal differences in induction of
heat-shock proteins in the water flea Daphnia magna.
Journal of Evolutionary Biology 18: 867–872.
Pijanowska, J. & M. Kloc, 2004. Daphnia response to preda-
tion threat involves heat-shock proteins and the actin and
tubulin cytoskeleton. Genesis 38: 81–86.
Reiter, R. J. & D. X. Tan, 2002. Melatonin: an antioxidant in
edible plants. Annals of the New York Academy of Sci-
ences 957: 341–344.
Reiter, R. J., D. X. Tan, W. Qi, L. C. Manchester, M. Kar-
bownik & J. R. Calvo, 2000. Pharmacology and physiol-
ogy of melatonin in the reduction of oxidative stress in
vivo. Biological Signals and Receptors 9: 160–171.
Reiter, R. J., D. X. Tan, M. J. Jou, A. Korkmaz, L. C. Man-
chester & S. D. Paredes, 2008. Biogenic amines in the
reduction of oxidative stress: melatonin and its metabo-
lites. Neuroendocrinology Letters 29: 391–398.
Ringelberg, J., 1999. The photobehaviour of Daphnia Spp.asa
model to explain diel vertical migration in zooplankton.
Biological Reviews 74: 397–423.
Slusarczyk, M. & E. Rygielska, 2004. Fish faeces as the pri-
mary source of chemical cues inducing fish avoidance
diapause in Daphnia magna. Hydrobiologia 526: 231–
234.
Tilden, A. R., M. A. Becker, L. L. Amma, J. Arciniega & A. K.
McGaw, 1997a. Melatonin production in an aerobic
photosynthetic bacterium: an evolutionarily early associ-
ation with darkness. Journal of Pineal Research 22: 102–
106.
Tilden, A. R., P. Rasmussen, R. M. Awantang, S. Furlan, J.
Goldstein, M. Palsgrove & A. Sauer, 1997b. Melatonin
cycle in the fiddler crab Uca pugilator and influence of
melatonin on limb regeneration. Journal of Pineal
Research 23: 142–147.
Tilden, A. R., R. Brauch, R. Ball, A. M. Janze, A. H. Ghaffari,
C. T. Sweeney, J. C. Yurek & R. L. Cooper, 2003.
Modulatory effects of melatonin on behavior, hemolymph
metabolites, and neurotransmitter release in crayfish.
Brain Research 992: 252–262.
Vivien-Roels, B. & P. Pe
´
vet, 1993. Melatonin: presence and
formation in invertebrates. Cellular and Molecular Life
Sciences 49: 642–647.
Yamano, H., Y. Watari, T. Arai & M. Takeda, 2001. Melatonin
in drinking water influences a circadian rhythm of loco-
motor activity in the house cricket, Acheta domesticus.
Journal of Insect Physiology 47: 943–949.
Yoshizawa, Y., K. Wakabayashi & T. Shinozawa, 1991.
Inhibition of planarian regeneration by melatonin. Hyd-
robiologia 227: 31–40.
50 Hydrobiologia (2010) 643:43–50
123