Download Why do brittle stars emit light? Behavioural and evolutionary

Cali. B iol. Mar. (2013) 54 : 729-734
Why do brittle stars emit light? Behavioural and evolutionary
approaches of bioluminescence
Alice JONES and Jérôm e M ALLEFET
M arine biology laboratory, Catholic University o f Louvain, 3 Place Croix du Sud, B ox L 7 .06.04,
B -134S Louvain-la-Nettve, Belgium. Fax: + 32 (0)10 47 34 76, E-fnail: alice.jones(cb.uclouvain.be
A b s tra c t: In this study, we investigated the functions o f biolum inescence (the production o f light b y living organism s) in
five brittle star species. Bioliuninescence is a w idespread phenom enon in the marine environm ent, and is especially
abundant in the class Ophiuroidea. It is assum ed that light in marine invertebrates m ainly plays a role o f defense against
predation, and many m echanism s o f defense have been proposed for brittle stars. We investigated the potential functions o f
startle effect (use o f light to deter predator), use o f light to advertise a predator that the prey is toxic (aposem atic signal)
and attraction o f a secondary predator (function usually called “burglar-alarm effect”). Predatory experim ents, involving
one or tw o predators trom different trophic levels allow ed us determ ining benefits o f the light em ission fo r several brittle
star species. We clearly dem onstrated that the three functions cited behind are used in brittle stars. It is clear now that brittle
stars use a w ide variety o f defensive m echanism s involving light.
R é su m é : Pourquoi les ophiures émettent-elles de la lumière ? Approches com portem entales et évolutionnistes de la
hiolum inescence. Cette étude porte sur les fonctions de la biolum inescence (la prodùction de lum ière p ar des organism es
vivants) chez cinq espèces d ’ophiures. La biolum inescence est mi phénom ène courant dans le m ilieu m arin, et il est
particulièrem ent abondant dans la classe des ophiuridés. Il est adm is que la biolum inescence joue un rôle de défense contre
la prédation chez les invertébrés benthiques. Plusieurs m écanism es de défense ont été suggérés pour les ophiures. Nous
avons investigues les fonctions potentielles de “startle effect” (répulsion du prédateur par la lum ière), d ’utilisation de la
lum ière pour prévenir le prédateur que sa proie est toxique (signal aposém atique) et d ’attraction d ’un prédateur secondaire
(fonction com m uném ent appelée “burglar-alarm ” ) ont été testées. Des expériences de prédation, faisant intervenir des
prédateurs d ’u n ou deux niveaux trophiques, nous ont perm is de situer les bénéfices associés à ré m issio n de lum ière pour
plusieurs espèces d’ophiures. Les trois fonctions citées plus haut ont pu être clairem ent dém ontrées chez les ophiures. II est
m aintenant clair que les ophiures utilisent une grande variété de m écanism es de défense im pliquant la lum ière.
Keyw ords: Biolum inescence • Ophiuroid • À posem atism • Burglar-alarm • Ethology
Introduction
Biolum inesccnce, the emission o f visible light by living
organism s (for a review see Haddock et al., 2010), is a
com m on feature in echinoderm s, especially in brittle stars.
in this class, at least 77 luminous species are known
(M allefet, 2012), o f 222 species tested, with a total o f 2,128
species and subspecies described (Stöhr 8c O ’Hara, 2012).
This abundance o f lum inous species, discovered recently
(M allefet, 2012) suggests th at lig h t production has
im portant functions in these organism s. Functions o f
biolum inescence can be divided in three categories:
intraspecific com m unication, help w ith predation, and
defense against predation. Studies suggest that the function
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FU N C T IO N OF O PH IU RO ÏD L U M IN ESC EN C E
o f biolum inescence in brittle stars involve defense against
predation (H erring, 1.995), such as startle effect (deterrence
o f predators by intense flashes), sacrificial lure (autotomy
o f a lum inous distal part o f arm s w hen attacked),
aposem atism (use o f a conspicuous signal to advertise
predators that the prey is toxic or unpalatable), or burglar
alarm effect (use o f light to attract secondary predator).
We investigated the biolurninescence functions in five
lum inous ophiuroids w ith prey -p red ato r experim ents:
A m phiura arcystata (H .L. Clark, 1911), A m phipholis
squam ata (D elle C hiaje, 1828), O phiocom ina nigra
(Abildgaard, in O.F. Müller, 1789), Ophiopsila aranea
(Forbes, 1843) and O phiopsila californica (A.H, Clark,
1921). These species differ in their lum inous pattern and
colour. W hile O. aranea and 0 . californica are known to
emit intense green flashes, the lum inous signal o f A.
squam ata is far lower. O phiocom ina nigra emits very weak
luminous m ucus w hen disturbed (Fontaine, 1964). The last
species, A, arcystata, em its a blue light. Finally, a sixth
species, O phiothrix fra g ilis (A bildgaard, in. O.F. Müller,
1789) w as used as non biolum inescent control.
As predator, we chose the crab Carcinus m aenas
(Linnaeus, 1758). This species is comm on in both the North
Sea and in the M editerranean Sea. M oreover, this species
was interesting because it is known to prey on echinoderms
(M untz el al„ 1965). Crabs w ere used sighted or blinded, to
com pare behaviour betw een crabs able or unable to see
biolum inescence. A secondary predator, the fish Diplodus
vulgaris (G eoffroy Saint-Hilairc, 1817), com mon in the
M editerran ean Sea, w as u sed for burglar alarm
experim ents, because it preys on crabs (pers. Obs.).
M any experim ents are conceivable to asses i f .
biolum inescence is involved in defensive functions in
ophiuroids. If light is used to deter predator, bioluminescent
prey should suffer lower predation than non bioiuminescent
ones w hen bioluminescence is visible, m eaning during the
night and w ith sighted crabs. I f light- is used to advertise
predators that the ophiuroid is toxic or unpalatable
(aposematic signal), it means that, on one hand, ophiuroids
arc unpalatable and, on the other hand, predator are able to
associated the ophiuroid unpalatability with its luminous
signal. Finally, if light is used to attract a secondary predator,
it means that the prim ary predator (the crab) should be more
predated by t,he secondary predator (the fish) when a
luminous ophiuroid is present. It means also that the ophi­
uroid should be less predated when the fish is present.
O ur experim ents on ophiuroids can then be listed as a set
o f questions:
• Does ophiuroid biolum inescence deter predators?
• Does ophiuroid biolum inescence advertise predators?
(i) A re ophiuroids unpalatable?
(ii) A re predators able to associate unpalatability and
lum inous signal?
• Does ophiuroid bioluminescence attract a secondary
predator?
Material and M ethods
Sam pling
Brittle stars were collected between 2007 and 2012 in
France and in California. Ophiopsila aranea was collected
at ARAGO marine station at B anyuls-sur-m er (France)
using SCUBA, and 0 . nigra and A. squam ata w ere
collected in N orth France, Wimeretix, by trawl and directly
on the shore, respectively. The non-biolum inesccnt control
species O, fragilis was also collected in W im ereux by trawl.
Ophiopsila californica and A, arcystata were collected in
Santa B arbara cam pus, U niversity o f C alifo rnia, by
SCUBA. Predators, crabs Carcinus m aenas and the fish
D iplodus vulgaris were collected in W im ereux and
Banyuls, respectively.
D oes ophiuroid bioluminescence deter predators?
To determine the potential deterrent effect o f light for
predators, experiments were run on the five lum inous
brittle star species. Crabs C. m aenas w ere u se d as
predators. For each test a brittle star and a crab w ere put in
contact in an aquarium o f 601, with a stone in tile center to
provide shelter. Each experiment lasts 12 hours, and was
repeated six times during the day, and six tim es during the
night with each species. The ophiuroids w ere w eighed
before and after to estimate the amount o f tissue lost during
the experiment. This index (weight o f brittle star eaten) was,
standardized by the weight o f the predator and called
“predation rate”; Experiments were repeated during a
day/night cycle, to highlight a possible influence o f the
bioluminescence on the predatory behaviour o f the crabs in
the dark, w hen it is the m ost clearly seen. We also ran this
experim ent with blinded crabs. Experim ents were repeated
w ith blinded crabs six times during the day and six tim es
during the night. Crabs were blinded by painting the distal
part o f the eyestalk black, with nail polish, as used in other
studies (for example see Duffy et al., 2006).
D oes ophiuroid bioluminescence advertise predators?
(i) Are ophiuroids unpalatable?
A posem atism is the use o f light or bright colors to warn a
predator that the prey is toxic or unpalatable. Since
association betw een a conspicuous signal and unpalatabili­
ty is required for this to work, w e investigated the
palatability o f the brittle star species. Tissues (arm s) o f the
ophiuroids were mixed w ith agar to form blocks. B locks o f
agar m ixed with fish pieces were also m ade, lo verify that
agar itself has no deterrent effect since fish is the com m on
731
A. JONHS, J. M A LL EFE T
crab diet in the laboratory. Each block was provided to a
crab for 30 m in, in a small aquarium o f 10 I. Each block
w as w eighed before and after the experiment, in order to
evaluate the am ount o f agar eaten. This index, standardized
b y the w eight o f the predator, was called consum ption rate.
T he handling time o f the block by the crab, and the
co n su m p tio n rate, w ere recorded as indicators o f
palatability (the longer and the more the block is handled
and consum ed, the more palatable is the species).
D o es ophiuroid bioluminescence advertise predators?
(¡i) Are predators able to associate unpalatability and
lum inous signal?
To study aposematism, we used the species O. nigra and the
species O. fragilis as non bioluminescent control. Crabs were
placed in contact repeatedly with the ophiuroid, to see if the
crab w ould avoid the ophiuroid after the emission o f light,
w h ich w ould suggest aposem atic use o f the bioluminescence. One brittle star and one crab were put on a
sm all aquarium (10 1) during four successive trials o f 30
minutes. Betw een'tw o trials, the brittle star was removed for
20 m inutes. The consumption o f brittle star was recorded for
each trial. Experiments were a m six times during the day and
six times during the night with both ophiuroid species, to
distinguish the effect o f the biolum inescence. Indeed,
biolum inescence is visible for the crabs only at night.
Experim ents w ere also run during the day to verify that no
other deterrent mechanisms were involved in the avoidance
learning.
D o e s ophiu ro id biolum inescence attract a secondary
p red a to r?
Finally, w e studied burglar alarm effect on O. aranea (using
O, fra g ilis as non-bioluminescent control species). We put in
contact brittle stars and predators from two different trophic
levels (crabs C. maenas as primary predator, and fish D.
vulgaris as secondary one). D ifferent prey-predators
com binations were tested to assess the predation on brittle
stars by crabs, fishes and both predators together. Predation
rate on crabs by the fishes, in the presence or absence o f
lum inous brittle stars, was also tested. Predatory experiments
took place in a 100 1 aquarium, during 12 hours. Each preypredator com bination was repeatedly tested six times during
the day, and six times during the night,
Statistica l analysis
A ll analyses w ere performed in JMP 8 or 10, using analysis
o f variance and multiple m ean com parison test (HSD
Tukey). Significance was always tested with the probability
o f 0.05 ( P < 0.05).
Results
Does ophiuroid biolum inescence deter predators?
Figure 1 illustrates the general effect o f biolum inescence as
a w ay o f defense against predation. C om parisons betw een
luminous and non-lum inous species, as w ell as blinded and
sighted crabs allow us to estim ate the efficiency o f light as
a defense against predation on a day/night cycle. We
observed that w ith sighted crabs, the predation rale is
always significantly higher during the day than during the
night, w ith luminous brittle star species. With the nonluminous species, we observed the opposite result, although
w ithout
significant
differences.
P redation
rates
significantly increase w ith the blind crabs during the night,
w hich indicates that vision o f biolum inescence is efficient
to reduce predation.
O. aranea
wt
b
nt
■F
O. nigra
O. californica
A. arcystata
A squamata
Ö. fragilis
b
■*
B . ■P
■pp—
0
0.05
0.1
0
0.05
0.1
Predation rate
F ig u re 1. Predation rates for blind or sighted crabs, during day
and night. HSD Tuckey, differen t letters in d icate strongly
different m eans, n —6 for each com bination.
D oes ophiuroid biolum inescence advertise p red a to rs?
(i) A re ophiuroids unpalatable?
Figure 2 shows the consum ption rate o f agar blocks made
w ith different brittle star species. C onsum ption
significantly differs according to the species (F K47 =
20.195, p < 0.001). Lower consum ption rate are observed in
four species: O. aranea, O. californica, O. nigra after
m echanical stress an d ri, arcystata.
FU N C T IO N OF O PH IU R O ID LU M IN ESC EN C E
732
0,1
D oes ophiuroid biolum inescence a ttra ct a secondary
predator?
0.09
o.os
ab
0.07
0.0Û
0,05
0.04
003
0.Q2 i
n
Q .O i
0 . aranea
ö. .
californita
O .níB ft
0 . nigra
A.
A .arcystata Oíraglllí
dfstwrbad squam ata
Fish
F ig u re 2. C onsum ption rates o f agar blocks. HSD Tuckcy,
different letters indicate strongly different m eans, n = 6 for each
com bination.
Figure 4A. shows predation rate on crabs, fo r different
prey-predator combination: crab-fish; crab-fishriiiininous
brittle star and crab-fish-non luminous brittle star, for
experiments in day and night period. D uring the day, crabs
are more predated for combinations including a brittle star.
No significant differences appear betw een com bination
with the luminous or the non-luminous ophiuroid. D uring
the night, predation on crabs increases significantly in the
combination with the luminous brittle star, but hot w ith the
non-lum inous species.
Results for predation suffered by brittle stars (Fig. 4B)
show no significant differences betw een com binations
(brittle star-crabs; brittle star-fish; brittle star-crab-fish)
neither during the day nor during the night.
D oes ophiuroid biolum inescence advertise predators?
M
(ii) A re predators able to associate unpalatability and
lum inous sig n a l?
D uring successive trials, it appears that the predation rate is
higher for O, fra g ilis than for O. nigra, w hatever the trial or
the p eriod (experim ent ran d uring day or night)
(F | Q4 = 10.267, p = 0.002). M ultiple mean comparisons test
shows that strong differences betw een predation in the
successive trials appear in two com binations: with the
species O. nigra during the night, and w ith the species O.
fra g ilis during the day. F or O. nigra during the night, the
consum ption o f brittle star is significantly higher during the
first trial than during the tw o last trials, where the
consum ption is null. For the com bination 0 . fragilis!day,
predation rate is higher fór the third trial. N o differences
betw een trials appear for O, nigra diuing the day or for 0 .
fra g ilis during the night (Fig. 3).
C.M o w w í
ù. VJtQBfitlï’*predator)
&tjrpnW(iümm9vs0f«y)
-X"
luminoyjpfcy)
OT *vr
im
tt- N
M 'X
V-
»«f * * g *
F ig u r e 4. A. P red atio n on the prim ary, p re d a to r (crab
C a m e n a s). HSD Tuckey, different letters indicate strongly
different means n - 6 for each com bination). B. Predation on the
brittle stars (ophiuroid O, aranea). HSD Tuckey, different letters
indicate strongly different m eans n - 6 for each com bination.
Discussion
Does ophiuroid bioluminescence deter predators?
È
J1±2 1 4
Day
0, n ig ra
Q .fragtils
F ig u re 3. Predation rates during successive trials. HSD
Tuckey, different letters indicate strongly different m eans, n = 6
for each com bination.
Predation experim ents were u n dertaken to address
questions o f the function o f the biolum inescence in
ophiuroids. Brittle stars are vulnerable to predation at night
with sighted crabs. This is uncom m on since crabs are
com m only nocturnal predators. In contrast, this difference
in predation rate and consumption disappears w ith blinded
crab. Hence the predation experiments strongly suggest that
the five luminous species exhibit a visual signal o f defense
against their predators. The biolum inescence is thus most
likely involved in the defense against predation in these
species. D uring the day, there was no difference in
predation o f luminous brittle stars and the control species
A. JO N ES, J. M A LL EFE T
O. fra g ilis, In addition, predation by blinded crabs does not
differ betw een day and night. These results indicate that
defense against predation in these ophiuroids are based on
vision. N o other anti-predatory strategies such as chemical
defenses seem sufficient to deter predators w ithout the
biolum inescence.
D o e s ophiuroid bioluminescence advertise predators?
(i) A re ophiuroids unpalatable?
T he palatability tests delivered interesting and surprising
results. The palatability o f O. aranea, A, arcystata and 0.
californica w as low. Concerning 0 . nigra, the palatability
is strongly m odified by the release o f m ucus w hich has a
strong deten*ent effect on the crabs. In absence o f the
released m ucus, the tissue o f 0 , nigra is eaten as m uch as
tissue o f 0 . fra g ilis or fish. We can conclude that the
m echanical stress induces the release o f mucus, and that
this mucus, includes both a visual w ay o f defense, the
biolum inescence, and a deterrent com ponent These data
su p p o rt the hypothesis o f the aposem atic use o f
biolum inescence. A posem atic use o f biolum inescence has
already been demonstrated for firefly larvae (De Cock &
M atthysen, 2001 & 2ÖÖ3), for millipedes (M arek et ah,
2011) and in the brittle star species Ophiopsila aranea
(Jones & Mallefet, 2010) and Ophiopsila riseii Llitken,
1859 (Grober, 1988), however controversy rem ains for this
study (G uilford & Cuthill, 1989; Grober, 1989). The two
brittle star species emit green intense flashes, a very
d iffe re n t lum inous pattern than O. n ig ra , but the
Lam pyridae larvae and millipeds (M arek et aL, 2011) emit
slow glow ing light, which gets closer to the pattern o f O,
n ig ra (D e C ock Sc M atthysen, 2001). E volution o f
aposem atic signals requires precise conditions concerning
appearance o f the signal as well as its m aintenance (Leimar
et al., 1986). O nly low value prey (i.e. toxic or unpalatable
prey) can evolve aposematic display. Regarding these
palatability tests, this seems to be the case with m echanical­
ly stim ulated O. nigra,'Secondly, aposematic prey should
suffer a low er predation rate than cryptic species. Predation
experim ents show ed that also this condition is fulfilled for
O. n ig ra . Finally, aposematic displays should allow the
avoidance learning, o f the predator.
D o es ophiuroid bioluminescence advertise predators?
(ii) A re predators able to associate unpalatability and
lum inous signal?
W hen a crab is repeatedly in contact with O. nigra, during
tile night, its consum ption o f brittle star significantly
decreases along the trials. It seems that the crab actually
avoids the prey, after two trials o f 30 minutes. In contrast,
this difference does not appear during the day, w hen
biolum inescence is not visible. The consumption does not
733
decrease w ith the control brittle star O, fra g ilis, w hich
proves that the decrease in the first case cannot be
explained by the satiety o f the crab. Avoidance learning
also occurs with Ophiopsila aranea and O phiopsila riseii,
but after only one trial (Grober, 1988; Jones & M allefet,
2010), which suggests that their strong signal m ay be m ore
effective. The use o f selective light signals as aposem atic
signals includes undeniable advantages. Actually, the light
is em itted only after disturbance, for O. aranea and O. riseii
as well as for O. nigra. The prey rem ains cryptic w hen not
disturbed, and does not suffer the costs o f an increased
detectability by naïve predators, which is a w ell-know n
problem in the explanation o f the evolution o f aposem atic
display (Eisner 8c Grant, 1981; G uilford & D aw kins, 1993;
Speed 8c Ruxton, 2005). Thus O. nigra has an im portant
advantage over the two other species.-Actually, the signal
and the deterrent com ponent are both present in the sticky
m ucus excreted outside the body w hen attacked. Here O.
nigra takes advantage o f its defensive m echanism deterring
its predator at the earlier stage o f their interaction. The
em ission o f luminous mucus, after disturbance, seem s to be
an advantageous strategy for aposem atic displays. H ow ever
patterns differ strongly am ong brittle stars w ith luminous
emission, aposematic use o f light seem s to include many
evolutionary
advantages,
and
this
function
of
biolum inescence may have been underestim ated in the past,
Further investigations, with other brittle star species, w ould
allow generalizing the function o f light for these organisms
and tackling the question o f the light function conservation
in this class o f echinodertns.
D oes ophiuroid biolum inescence a ttra ct a secondary
predator?
O ur observations concerning interactions betw een
luminous brittle stars, crabs and fishes support the burglar
alarm hypothesis. Indeed, during the night, the predation on
crab by the fish is higher if O . aranea is present. This
clearly indicates that light em itted by O. aranea can
advertise the presence o f the crab to a predatory fish.
D uring the day, w e observe thai predation rate on the crab
increases when a brittle star is present, no m atter w hether
the brittle star is lum inous or not. Since biolum inescence is
not visible during the day, it sim ply indicates that hunting
ophiuroids makes the crab less cryptic during the day hence
m ore available for the fish.
We also recorded predation rates on O. aranea. In this
case, w e do not observe any difference betw een
combinations. The predation rate on the brittle star is low er
during night than day, but does not decrease w hen predators
o f the two levels are present, contrary to w hat is predicted
by the theory, i.e. lower predation rate on the luminous
brittle star due to higher predation on the prim ary predator.
These results support the use o f biolum inescence as
734
FU N C T IO N OF O PH IU RO ID L U M IN ESC EN C E
burglar-alarm signal for 0 . a r a n e a , but w e suggest that the
benefits o f this function m ight be visible at the level o f the
population not for the single individual. Studies o f the
genetic structure o f the Banyuls 0 . aranea population
should in the future allow us to determ ine if a kin-selected
function o f biolum inescence is conceivable for this species.
The use o f light as burglar alarm signal has also been high­
lighted in dinoflagcllatcs (M cnsingcr Sc Case, 1992;
Abraham s & Townsend, 1993), and suggested by Robison
(1992) in the holothurian species E nypniastes eximia
(Théel, 1882).
In conclusion, this study illustrates the diversity of
mechanism s involved in the use o f light as a defense
against predation in brittle stars. This diversity should
explain why this feature is so w idespread in the class
Ophiuroidea. M oreover, besides the defensive function, it
w ould b e v ery in terestin g to study oth er roles o f
biolum inescence (such as help for predation or intraspecific
com m unication...) in this class to increase the information
concerning the function o f biolum inescence in brittle stars.
A cknow ledgem ents
This project was financially supported by the ASSEM BLE
program m e o f the European Community, grant agreement
no. 227799, for the access to the M arine Station Arago o f
Banyul.s-sur-M.er. The authors also thank the University o f
Santa B arbara for collaboration in the sam pling o f 0 .
californica. This w ork was supported by a grant from de
F N R S -F R IA to A. Jones. J. M allefet is a research associate
o f the FN RS. This is a contribution to the Biodiversity
R esearch Center (BDIV).
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