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THE JOURNAL OF EXPERIMENTAL ZOOLOGY 275339-345 (1996)
Serotonin Involvement in Larval Settlement of the
Barnacle, Balanus amphitrite
HISASHI YAMAMOTO, AKIKO TACHIBANA, SATORU KAWAII,
KIYOTAKA MATSUMURA, AND NOBUHIRO FUSETANI
Fusetani Biofouling Project, ERATO, JRDC,Niigata Engineering Co. Ltd.,
Isogo, Yokohama 235, Japan
ABSTRACT
Following our previous report (Yamamoto et al. r19951 Zool. Sci., 12:391-396) in
which we demonstrated that protein kinase C (PKC) plays an important role in larval metamorphosis of the barnacle Balanus amphitrite, we examined the effects of a range of neurotransmitters, including serotonin (5-hydro~ytryptamine)~
epinephrine, and norepinephrine on cyprid
settlement and metamorphosis. Serotonin induced pronounced larval settlement. Furthermore,
settlement was inhibited by neurotransmitter uptake blockers, such as amitriptyline, imipramine,
and desipramine, in a concentration-dependent manner. Cyprids exposed t o these uptake blockers
metamorphosed without settling on substrata. These results suggest that serotonin is involved in
larval settlement. 0 1996 Wiley-Liss, Inc.
Settlement competent larvae of sessile marine
invertebrates, such as barnacles, mussels, and hydroids, are believed to initiate settlement behavior upon reception of chemical cues which are often
derived from adult conspecifics or from prey organisms (Morse, '90). Cyprid larvae of barnacles
have long been known to respond to protein found
i n conspecific adults, known as arthropodin
(Larman et al., '82). When exposed to adult extracts, cyprids usually begin to explore potential
settlement substrata and eventually settle by secreting cement substance, after which metamorphosis to the juvenile barnacles takes place. It is
probable that signal reception followed by signal
transduction is a n integral part of this sequence.
However, very little is known about the receptors
or signal transduction systems involved.
A receptor coupled with G-protein has, however,
been suggested as the signal reception system in
veliger larvae of the red abalone Haliotis rufescens
(Baxter and Morse, '92). A number of neurotransmitters including dopamine, epinephrine, and
norepinephrine have further been reported as inducers of larval settlement and metamorphosis in
a range of marine invertebrates (Jensen and
Morse, '90; Pawlik, '90; Pires and Hadfield, '91).
However, it is unclear whether these neurotransmitters bind to receptors to induce metamorphosis, and no receptor molecules have as yet been
isolated from marine invertebrate larvae (Morse,
'90). Larvae of the hydroid Hydractinia echinata,
by contrast, have been reported to metamorphose
when exposed to phorbol esters, suggesting the
0 1996 WILEY-LISS, INC.
involvement of a protein kinase C (PKC) signal
transduction system in the metamorphosis of
these larvae (Leitz and Klingmann, '90; Leitz and
Muller, '87; Muller, '85; Schneider and Leitz, '94).
We have already demonstrated that a PKC signal transduction system plays a n important role
in larval metamorphosis of the barnacle Balanus
amphitrite (Yamamoto et al., '95). Furthermore,
recent evidence has demonstrated the involvement
of cyclic AMP in the settlement of this species
(Clare et al., '95). In order to clarify the operation
of signal transduction systems in cyprid larvae,
we further examined the effects of a range of neurotransmitters on settlement and metamorphosis.
MATERIALS AND METHODS
Materials
Artificial seawater (ASW) was prepared according to the Van't Hoff formula as follows: 460 mM
NaC1, 10.1 mM KCl, 9.2 mM CaCl,, 35.9 mM
MgC12, 17.5 mM MgS04, and 10 mM Tris-HC1 (pH
8.2). Serotonin, epinephrine, norepinephrine, and
quinacrine were purchased from Sigma Chemical
Co. (St. Louis, MO). GABA (y-4-amino-n-butyric
acid), L-DOPA (L-p-3,4-dihydroxyphenylalanine),
dopamine, amitriptyline, imipramine, and desipramine were purchased from Wako Pure-
Received August 29, 1995; revision accepted March 12, 1996.
Address reprint requests to Hisashi Yamamoto, Fusetani Biofouling
Project, ERATO, JRDC, c/o Niigata Engineering Co. Ltd., Isogo,
Yokohama 235, Japan.
340
H. Y-OTO
chemicals Co. (Osaka, fJapan). Octopamine was
obtained from Aldrich Chemical Co. (Milwaukee, WI).
Larval settlement assays
Competent cyprid larvae were obtained from
laboratory cultured adu It Balanus amphitrite using methods described previously (Yamamoto et
al., '95). Settlement assays were performed using
six-well polystyrene plates (Corning Cell Wells,
Corning, NY).Six milliliters of ASW (see Materials) was added to each well, plus 10 2 2 cyprid
larvae. The plates were then placed on a n orbital
shaker at 22°C. Test solutions were prepared by
the addition of 6 ~1 of aqueous or diluted HCl solution to 6 ml of ASW in each well. Epinephrine
and L-DOPA were dissolved in dilute HC1, but HCl
alone had no effect on cyprids at concentrations
of up t o 1 x 10" M. Plates were observed daily
for 5 or 6 days under a binocular dissection microscope. Daily counts were made of the numbers
of settled and metamorphosed larvae in each well.
Significant effects on l a r d settlement were tested
using analysis of variance (ANOVA), following
which Tukey-Kramer multiple comparison tests
(at P < 0.05) were used t,o identify specific effects.
Microinjection of cyprid larva
Larval movement was restrained by overnight
storage at 4"C, following;which cyprids were fixed
loosely between two glass coverslips. Microinjection was performed as Tollows: a 7 pm diameter
glass micropipette containing test solution was
held by a micromanipulator allowing peritoneal
(intraantennular) injection of cyprids. Injected
cyprids were immediately transferred to six-well
polystyrene plates (one cyprid/well) containing 6
ml of ASW, and plates were then placed on a n
orbital shaker at 22°C. The volume of test solution microinjected into each cyprid was determined by the fluorescence intensity of quinacrine
(Ex/Em: 380/540). When quinacrine solution at a
concentration of 10 mM was injected in a cyprid
larva, the final concentration of quinacrine within
the cyprid was calculated as approximately 20 pM
(500 x dilution). Each dlrug treatment was replicated at least five times.
ET AL.
A
100
z 0o
+serotonin
Q - norepinephrine
--X--epinephrine
-
r
T
r
0
0.1
1
10
100
conc. [ pM ]
B
l o80
o
c
- Q- - L-DOPA
Fig. 1. A: Effects of 0.1-100 FM serotonin, epinephrine,
and norepinephrine on B. amphitrite cyprid larval settlement.
B: Effects of 0.1-100 FM GABA, L-DOPA, dopamine, and
octopamine on B. amphitrite cyprid larval settlement. Data
presented are means f S.D.
With the exception of epinephrine (F = 1.3430, ns),
all drugs tested were found to have a highly significant effect on the settlement of B. amphitrite
cyprids over the range of concentrations tested
(Table 1).Statistical significance was as follows
(ANOVA): serotonin (F = 23.4958, P < O.OOOl),
norepinephrine (F = 4.5896, P < O.OOl), GABA (F
= 13.4492, P < O.OOOl), L-DOPA (F = 105.5102, P
< O.OOOl), dopamine (F = 90.6277, P < O.OOOl),
octopamine (F = 219.0287, P < 0.0001). However,
serotonin promoted cyprid settlement at concentrations of 100 pM, while other neurotransmitters had no settlement-promoting effects. The time
RESULTS
course of cyprid settlement promoted by serotoLarval settlement assays
nin is presented in Figure 2. Statistical signifiThe effects of various neurotransmitters, includ- cance at each concentration of serotonin over 5
ing serotonin, epinephrine, and norepinephrine, days was observed as follows (ANOVA): day 1 (F
on the larval settlement and metamorphosis of = 12.1598, P c O.OOOl), day 2 (F = 32.1722, P <
Balanus amphitrite are presented in Figure 1. O.OOOl), day 3 (F = 27.5201, P c O.OOOl), day 5 (F
341
SEROTONINAND BARNACLE SETTLEMENT
TABLE 1. Pairwise comparison for all neurotransmitters tested'
0
0.1
Serotonin
Norepinephrine
Epinephrine
GABA
L-DOPA
Dopamine
Octopamine
0
1
0
10
0
0
100
0.1
1
0.1
10
0.1
100
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
10
100
10
100 [pMl
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
'Statistical significancewas assessed at P = 0.05 (Tukey-Kramermultiple comparison test). 0, significantly different.
= 20.3872, P < 0.0001). During day 1, with the
exception of 0 and 0.1 pM, 0 and 1 yM, and 0.1
and 1 pM, all other painvise comparisons for serotonin were found t o be statistically significant.
On the second day, except for 0 and 10 pM and
0.1 and 1 @
all!I
comparisons
,
were significant.
On the third and fifth days, except for 0 and 1
pM, 0 and 10 yM, and 1 and 10 pM,all comparisons were significant. Within 5 days, all settled
larvae metamorphosed fully into juveniles. Induction of larval settlement by serotonin at low concentrations prompted examination of the effects
of serotonin uptake blockers on cyprids as follows:
amitriptyline (Hyttel et al., '80; Kriiger et al., '86),
imipramine (Barbaccia et al., '83; Barondes, '94;
Javaid et al., '79; Kruger et al., '86), and desipramine (Checkley et al., '81; Javaid et al., '79;
Lee et al., '83). All these well-known serotonergic
uptake blockers inhibited larval settlement at 10100 pM but promoted metamorphosis at 1-10 pM
(Fig. 3). Each serotonin uptake blocker treatment
was found to have a highly significant effect on
larval settlement (Fig. 3). Results of ANOVA were
100
unsettled juvenile
s loo
5
Y
.-
.-bP
.E
CI
s
-
I
c
60
-
40
Q
e
0.1
ASW
20
80
100
60
80
100
60
80
100
40
60
juvenile [YO]
- 100 1
h'
3
10
a,
.-c
E
.-E
1
0.1
E
iz
2.
a,
.-
0
20
0
20
40
juvenile [Oh]
loo
10
C
E
l
.G
0.1
!
40
a,
ASW
al
u,
1
0
Y
80
10
a,
E
c
r
20
0
Fig. 2. Effects of 0.1-100 pM serotonin on the time course
of B. amphitrite cyprid larval settlement. Data presented are
means -c S.D.
40
juvenile
[Oh]
Fig. 3. Effects of 0.1-100 pM serotonin uptake blockers
on B. amphitrite cyprid larval settlement and metamorphosis. Data presented are means f S.D.
342
H. YAMAMOTO ET AL.
as follows: amitriptyline (F = 336.1766, P <
O.OOOl), imipramine (F = 171.1640, P < O.OOOl),
desipramine (F = 154.3397, P < 0.0001). All three
treatments demonstrated a relatively high proportion of unsettled individuals at high concentrations of uptake blocker. This was less marked in
the case of desipramine, with which no unsettled
juveniles were observed below a concentration of
1 pM. Cyprids normally settle by attachment to
surface substrata by the secretion of cement substance, followed by metamorphosis to the juvenile
barnacle. However, although metamorphosis proceeded as observed in natural settlement, attachment to surface substrata did not take place when
cyprids were exposed to amitriptyline, imipramine,
and desipramine (Fig. 4).
Finally, we examined the effects of amitriptyline, imipramine, and desipramine on the activity of serotonin. These uptake blockers all
inhibited the activity of serotonin. A combination
of 1-100 pM serotonin and 1 pM serotonin uptake blockers produced larvae which were unable
to undergo settlement and attachment but were
still capable of full metamorphosis into juvenile
barnacles (Fig. 5 ) . While! combinations of serotonin and imipramine (F =I 1.4795, ns) and seroto-
nin and desipramine (F = 2.6429, ns) had no significant effects on settlement at the concentrations
employed, serotonin plus amitriptyline had a
highly significant effect (F = 50.5666, P < 0.0001)
on the number of larvae which settled and fully
metamorphosed into juveniles. Serotonin plus
amitriptyline also had the most pronounced effect on the production of unsettled juveniles (I? =
19.8128, P < O.OOOl), and production of the latter
was highest at 1 pM amitriptyline plus 100 pM
serotonin (Tukey-Kramer, P < 0.05). A similar pattern was observed for imipramine (F = 22.5714,
P < 0.0001); however, no significant effect was recorded for serotonin plus desipramine (F = 3.7377,
P = 0.0482), although the numers of unsettled larvae did differ significantly by pairwise comparison between 1:land 1:lOO (P < 0.05). These larvae
had the same appearance as those described in
Figure 4. For amitriptyline and imipramine, the
percentage of settled juveniles increased with increasing serotonin concentration. The agents
tested were nontoxic to cyprid larvae at concentrations of up to 10 pM. Most cyprids which failed
to settle and metamorphose did not die but did
eventually stop swimming, usually after 5 days.
Some cyprids died at concentrations of 100 pM;
however, this was a limited effect, and the majority of cyprids were still alive during assays.
Microinjection of cyprid larva
The cyprid microinjection process is presented
in Figure 6, and the results of settlement assays
I
settled juvenile
unsettled juvenile
I
ami+ 1
ami+ 10
ami+100
imi+ 1
h i + 10
imi+100
des+ 1
des+ 10
des+100
Fig. 4. B. amphitrite cyprid.s in ASW alone and following
treatment with 1 p M amitriptyline. a: Cyprid larva. b Normal settled juvenile. c: Unsettled juveniles resting on the bottom of experimental wells. Bar..300 pm.
I
0
20
tM
I
40
60
juvenile [%]
I
I
80
100
Fig, 5. Inhibition of 1-100 ,LLMserotonin activity by 1yM
serotonin uptake blockers in B. amphitrite cyprid larvae. Data
presented are means c S.D. ami, 1 pM amitriptyline; imi, 1
pM imipramine; des, 1 pM desipramine; 1, 10, 100, serotonin
concentration (pM).
SEROTONINAND BARNACLE SETTLEMENT
343
conducted using injected cyprids are presented in
Table 2. Only serotonin induced larval settlement,
whereas the other neurotransmitters demonstrated no such effect, with the exception of a
single cyprid which metamorphosed following microinjection with dopamine. When using the microinjection assay, the results of drug treatments
were the same as those already obtained using
the routine plate assays. Following microinjection
with ASW alone, 2/8 cyprids settled and metamorphosed. Similarly, a single cyprid (1/9>settled and
metamorphosed following injection with dopamine. Moreover, as in previous trials using external reagents, serotonergic uptake blockers induced
nonsettled, nonattached, but fully metamorphosed
juveniles. Quinacrine and the other neurotransmitters tested had no effect on cyprids. Following
microinjection, most cyprids were either still actively swimming, resting on the bottom surface
of the experimental wells, or floating at the water surface and therefore appeared to have been
unharmed by the microinjection process.
DISCUSSION
It is widely believed that the process of larval
settlement and metamorphosis in marine invertebrates can be described by the following process:
exogenous chemical cues bind to chemosensory receptors on the larva, resulting in signal transduction by neurotransmitter to the interior cells,
which leads t o cement secretion. Hitherto, no receptor molecules have been isolated from marine
invertebrate larvae (Morse, '90).
In barnacles, competent cyprid larvae initially
swim and then crawl in search of appropriate
TABLE 2. Results of trials in which B. amphitrite cyprids
were microinjected with a variety of neurotransmitters and
serotonin uvtake blockers Cn 2 6j1
Settled Unsettled
juvenile juvenile
5 rnM (10 pM, n = 6)
50 mM (100 pM, n = 6)
100 mM (200 pM, n = 9)
Epinephrine
100 mM (200 pM, n = 6)
Norepinephrine 100 mM (200 pM,n = 6)
GABA
100 mM (200 pM, n = 9)
L-DOPA
100 mM (200pM, n = 9)
Dopamine
100 mM (200 pM, n = 9)
Octopamine
100 mM (200 pM, n = 6)
Amitriptyline
5 mM (10 pM, n = 9)
Imipramine
5 mM (10 pM, n = 12)
Desipramine
5 mM (10 pM, n = 6)
ASW
in = 8)
Serotonin
Fig. 6. Microinjection of a B. amphitrite cyprid. a: Microinjection of cyprid larvae was performed by the insertion of a 7 pm diameter glass micropipette containing test
solution. b: Cyprid following microinjection with test solution. Cyprids appeared unharmed by the microinjection
process. Bar, 300 pm.
2
4
6
0
0
0
0
1
0
0
0
0
2
0
0
0
0
0
0
0
0
0
8
9
4
0
'(pM, n), (approximate internal agent concentration, sample size)
344
H. YAMAMOTO ET AL.
settlement substrata arid finally settle on a suitable settlement site where they then attach and
metamorphose (Crisp, '84;Walker et al., '87). Larval settlement and metamorphosis are often influenced by a range of environmental and synthetic
factors which have been reported as follows: settlement surface color (Yule and Walker, '841,water
movement (Crisp, '55), conspecific adult-derived
proteins (Larman et al., '821, synthetic peptide analogs of barnacles settlement pheromone (Tegtmeyer
and Rittschof, '861, and bacterial films (Maki et al.,
'90). In addition t o these exogenous factors, the
involvement of signal tra nsduction systems including PKC (Yamamoto et al., '95) and CAMP(Clare
et al., '95) have also been reported. More than this,
however, little is known about the signal transduction systems involved.
Various neurotransmjtters, including epinephrine, norepinephrine, and dopamine, have been
reported as settlement and metamorphosis inducers (Jensen and Morse, '90; Pawlik, '90; Pires and
Hadfield, '91). However, it is suggested that such
agents act directly on receptors of the larval nervous system of the red abalone (Huliotis rufescens
(Morse, '90). In the present study, we have demonstrated that serotonin induced cyprid larval
settlement (Figs. 1, 2), with 0.1 pM serotonin inhibiting cyprid settlement while 100 pM serotonin promoted it. These results suggest that there
may be two different kinds of serotonin binding
sites, with either high oir low affinities for serotonin. On exposure to 0.1 pM serotonin, high affinity binding sites may affect the inhibition of
serotonergic transduction. By contrast, when exposed t o 100 pM serotonin, low affinity binding
sites may affect the promotion of serotonergic
transduction. The serotonin uptake blockers, amitriptyline, imipramine, and desipramine (0.1-100
pM), were found to inhibit cyprid settlement and
metamorphosis. At lower concentrations, however,
these agents induced metamorphosis but not
settlement (Fig. 3). These results provide further
evidence that these upt,ake blockers may inhibit
serotonin binding in cylprids. In order t o clarify
these results, combinations of 1-100 pM serotonin
and 1 pM serotonin uptake blocker were examined
(Fig. 5). In the presence of 1 pM amitriptyline or
imipramine and 1-100 pM serotonin, percentages
of unsettled juveniles increased depending on increases in serotonin concentration. Desipramine
also induced unsettled juveniles; however, the percentages decreased dependent on increases in serotonin concentration. This difference may be due
to specificity of the serotonin binding block. It is
known that desipramine blocks not only serotonin uptake but also norepinephrine uptake (Lee
et al., '83). Our results suggested that desipramine
acted as a serotonin binding blocker, but its potency was not so strong as that of amitriptyline
and imipramine. Serotonin alone was found to promote settlement at 100 pM (Figs. 1, 2). Moreover,
induction of settlement by serotonin was inhibited by serotonergic uptake blockers such as amitriptyline, imipramine, and desipramine (Fig. 5 ) ,
indicating the involvement of serotonin in signal
transduction for settlement, while serotonin promoted general searching behavior. In addition,
these uptake blockers produced nonsettled but
fully metamorphosed juveniles. These results suggest that serotonin binding t o receptor is necessary for the natural cyprid settlement process.
In order t o confirm the involvement of serotonin in cyprid settlement, serotonin and serotonergic uptake blockers were individually microinjected
into cyprids (Fig. 6). Injection of 50 mM serotonin
resulted in an internal concentration of approximately 100 pM in the cyprid, which was found t o
promote larval settlement in a dose-dependent
manner. However, 5 mM imipramine (calculated
as 10 pM imipramine in the cyprid) induced
nonattached, nonsettled juveniles. Microinjected
50 mM (100 pM in cyprid) serotonin uptake
blockers induced unsettled juveniles. Results obtained from the microinjection experiments, although generally similar to those obtained from the
routine settlement assays, were calculated to be approximately 500 times more sensitive (Table 2).
Serotonin is known t o mediate signal transduction in many invertebrates species, most notably in molluscs. It has been suggested that
serotonin activity is modulated by cAMP
(Deterre et al., '81; Walker, '851, and Clare et
al. ('95) have recently reported that cAMP was
involved in the pheromonal modulation of
cyprid settlement. Our results therefore provide
further evidence that a relationship exists between serotonin and cAMP in the larval settlement process in B. amphitrite.
In conclusion, serotonin induced cyprid settlement, which was inhibited by serotonin uptake
blockers, suggesting that serotonergic neurons
play an important role in the settlement of B.
amphitrite cyprids. A PKC signal transduction system is already known to be involved in the larval
metamorphosis of the same species (Yamamoto et
al., '95). The present results provide further evidence that settlement and metamorphosis may be
physiologically independent events in this species.
SEROTONINAND BARNACLE SETTLEMENT
ACKNOWLEDGMENTS
We thank Dr. C. G. Satuito, K. Natoyama, and
M. Yamazaki for their help with larval culture.
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