Bijdragen tot de Dierkunde, 50 (1): 87-95 — 1980
Meandrina meandrites and Emblemariopsis diaphana,
first record of an association between a stony coral and
a fish, similar to anemone/fish relationships
by
Maureen E. Butter Marlies Wapstra & Eric van Dijk
Institute of Taxonomie Zoology, University of Amsterdam, The Netherlands
&
Caribbean Marine Biological Institute (Carmabi), Curaçao, Netherlands Antilles
Abstract genus Emblemariopsis, Chaenopsidae (key to
and cf. 1963 and genera species, Stephens, described between Caribbean 1970), An association is a stony coral, and to be E. 1927. Meandrina meandrites, and a chaenopsid fish, Emblemariop- proved diaphana Longley,
sis diaphana. Like in anemone/fish associations the coral
tentacles provide shelter for the fish. Some observations were
made, both in the field and in the laboratory, of the behaviour RESEARCH AREA
of both fish and coral with respect to each other.
The made the majority of observations were at
S.W. coast of Curaçao, Netherlands Antilles, about INTRODUCTION 1 km East of Piscadera Bay. Some field charac-
teristics are given in fig. 1 and table I (after But- The symbiosis between pomacentrid fishes (mostly ter, 1979). The current is usually East-West, the and stoichactiid Amphiprion species) sea ane- clear water is fairly (usually about 25 m visibility, and mones in the Indopacific area is well known sometimes 10 m). extensively studied (cf. Mariscal, 1966, and
Allen, 1975, for general information). Recently
association Albrecht (1977) described an of about
fish 30 species, mostly juveniles or inconspicuous species, seeking shelter between the tentacles of the anemone Condylactis gigantea, in the Carib- bean.
similar has been Never, though, a symbiosis reported of a fish and a stony coral, although
coral do some species have rather long tentacles.
Such relation if it is a however, exists, likely to remain unnoticed, as most corals have their ten- Fig. 1. Profile of the reef, East of Piscadera Bay. tacles expanded only during the night. By chance,
the had from during a nightdive at Curaçao reef, we Apart this location the fishes were also
find the East of the good fortune to a small fish between seen immediately Piscadera (at night), on tentacles of Meandrina meandrites (Linnaeus, several colonies of Meandrina meandrites, be-
After closer Meandrina and and the 1758). inspection many tween 10 20 m depth one between appeared to be occupied by these fishes. This tentacles of Eusmilia fastigiata (Pallas, 1766) at
find do research about unique compelled us to some 10 m depth. Further, occasionally, 500 m
the the the after nature of relationship, results of West of Piscadera (by day) on Meandrina, be-
the and which are presented here. The fish belongs to tween 10 20 m depth. Also, in Santa Marta, 88 M. E. BUTTER ET AL. - CORAL/FISH ASSOCIATION
2. 21 Fig. Emblemariopsis diaphana Longley, 1927. Standard length mm.
Table I which low in we kept as intensity as possible, in
order to corals to of the reef of Piscadera the and minimize Composition East Bay, percentages keep expanded
of other influences of the coverage. any disturbing light.
4Vi m 12 m 22 m 30 m
(%) (%) (%) (%) RESULTS
Meandrina meundriles 19.9 6.4 3.8 3.9
4.8 Agaricia sp. 2.2 3.2 5.5 1. PHYSICAL CHARACTERS OF THE FISH Montastrea sp. 3.0 15.1 9.6 17.7
Rock, sand, algae 57.0 67.4 72.1 69.6 Standard Other 17.71) 7.8 9.6 3.3 Appearance (figs. 2-5).
length of captured specimens varied from 11 to !) An important hereof (6.6% coverage) is constituted part standard deviation 21.5 mm, mean 16 mm and of Madracis mirabilis (Duchassaing & Michelotti, 1861), at fishes are the other depths this species is entirely absent. 3 mm (of 28 specimens). Living translucent brownish, with red specks along the
Colombia: one fish, apparently the same species, lateral line and the anal fin base. The anterior part
on Meandrina, at 20 m depth, during the day. In of the dorsal fin has a heavier red pigmentation
Curaçao Meandrina meandrites is a rather com- than the rest of the fin. There are red blots along
Santa Marta is has red mon species, in it quite rare. the dorsal fin base and the visceral area a
coloration. The eyes are heavily pigmented, very
dark, being the most conspicuous part of the
METHODS of the is animal. Behind the eyes, on top head, a
conditions dark patch. Under natural light on the
with the aid of have colour Mean- Field observations were done reef they seem to the same as
At used diver's drina. alcohol formalin lose much of SCUBA gear. night we a lamp. In or they
could be Specimens captured by putting a plastic their pigmentation. bag around the coral and chasing the fish into
it. The thus collected fishes — were transferred to a Stomach content. Stomach contents
container with and of collected seawater transported to the were examined specimens one to two
for further hours and laboratory examination or aquarium after sunset, of specimens collected observation. For the latter, several tanks were set from two hours before to two hours after sunrise.
with sand with In and up a bottom, one Meandrina and most cases the stomach esophagus were
fishes in each. in ad- two The next few days their be- empty; if not, digestion was usually an
haviour studied was during the late afternoon, vanced stage. Small arthropods, diatoms, algae and
night and mid morning. For the nighttime obser- polychaetes could still be recognized. See also
make vations we had to use of artificial light, table II. BIJDRAGEN TOT DE DIERKUNDE, 50 (l) - 1980 89
Fig. 3. Emblemariopsis diaphana on Meandrina meandrites. Daytime, coral tentacles not expanded. Photograph Eric van Dijk.
Table II 2. BEHAVIOUR AND OCCURRENCE
Numbers and percentages of fishes with empty stomach and esophagus, in the early evening and in the early morning. 2.1. On the reef, at night
early early The coral. — By sunset Meandrina begins evening % morning % to expand its tentacles. During the whole night empty 13 68.4 6 31.6 the coral is with its 6 actively feeding, catching not empty 66.7 3 33.3 tentacles all kinds of swimming and suspended
1 2 "Early evening" is about to hours after sunset, "early organisms. At night these are abundantly present morning" refers to the period between 2 hours before and in the vicinity of the corals. Meandrina tentacles 2 hours after sunrise.
are about 2 cm those of Eusmilia are some- Most stomachs were empty, but 4 in the early evening and 3 long,
of in the early morning were in a stage advanced digestion, what longer. whereas only in 2 cases in the early evening the fish appeared If touches tentacle it is imme- prey a captured to have eaten recently. diately. Directly surrounding tentacles contract
— Some bore Each also into for Eggs. specimens eggs. ovary and pull the prey a stomodaeum contained about 20 diameter 0.2 to 0.5 further In of eggs, mm. consumption. case large prey a Of the 28 fishes examined, there were 6 ovigerous swelling remains visible at the colony surface. their standard ones, lengths were 13, 14, 14, 17, After a while the tentacles relax and expand again.
20 and 21.5 The the mm. larger prey, the longer the duration be- 90 M. E. BUTTER ET AL. - CORAL/FISH ASSOCIATION
Meandrina meandrites. coral tentacles Eric Fig. 4. Emblemariopsis diaphana on Nighttime, expanded. Photograph van Dijk.
The and it natans tween contraction and re-expansion. most was seen once on Colpophyllia
central These peripheral tentacles expand first, the most (Müller, 1775). two species are not un-
the tentacles evokes but less abundant than Mean- ones last. Any prey touching common, markedly
contraction if fails drina. Small Meandrina colonies contained either a response; capture (a rare few all. heads occurrence) the tentacles re-expand immediately. fish, or none at In large coral
there often individuals The consists of small most of were more: to ten were prey shrimps, up
them also lot of sometimes the about 3 mm, but up to 15 mm, a occupying same colony. Usually,
which the the distance them worms from 10 to 30 mm of larger between was not under 10 cm.
small ones are in mass comparable to the smaller com- Very specimens were hardly visible; prob-
and needle-like translucent the densities, as in table are mensal fishes, many ably presented 111, animals of about 10 mm. Other fishes, in size therefore underestimated.
the time the comparable to the species under investigation, Most of fishes were hiding be-
were not seen near Meandrina. tween the tentacles, at the bottom of an interstice
between two ridges (fig. 4). Sometimes they
Most moved few took The fish. fishes were found on on a centimeters, or position on
Meandrina, with the highest density at a depth top of a ridge; sometimes they emerged partly of 15 At 3-8 from the tentacles and then hid between m. m they were very scarce, though again
is abundant When Meandrina at these depths. Occasion- them (fig. 6). threatened (hand move-
three of the ally (in cases) they occurred on Eusmilia ments investigators), they fled between
if fastigiata (Pallas, 1766), as can be seen in fig. 5, the tentacles they were outside of the colony. BIJDRAGEN TOT DE DIERKUNDE, 50 (1) - 1980 91
Eusmilia Nighttime, coral tentacles Eric van Fig. 5. Emblemariopsis diaphana on fastigiata. expanded. Protograph Dijk.
III the moved Table If they were on colony, they just on a
little, between the tentacles. To chase a Counts of Meandrina meandrites at several depths and the staying number of fishes found on them. fish of the almost had away, out tentacles, one to
touch it, in such a way that the coral contracted
Number of fishes per coral its tentacles. Very small individuals reacted by 0 1 2 3 4 hiding deep between the septs and could not be depth (m) scared it them away, so was not possible to capture m 11 1 to 2 hours with our method. 15 1 4 1 2 after sunset When fish while between the ten- 221/2 8 2 1 a stayed a
tacles without moving, the tentacles slowly started
— 7l/2 10 1 — — 1 to 2 hours to envelop it. Then the fish made a sudden 15 7 4 2 1 before sunrise movement and the tentacles relaxed When 221/2 10 3 1 again.
of a fish was outside the colony, but within reach
In other dives, where corals were not systematically counted, the tentacles, the tentacles did not react. If at
have found corals with fishes. The we many more propor- close distance the fish prey was caught, rapidly tions in the beginning of the night do not differ significantly swam from those at the end of the night. away. M. E. BUTTER ET AL. - CORAL/FISH ASSOCIATION 92
movements already mentioned, they made casual
sudden order relax movements in to the envelop-
ing tentacles.
Moderately active behaviour involves the follow-
ing types of behaviour:
( 1 ) A small change of position, with intervals of Fig. 6. Hiding between the tentacles, coming out a little and of behaviour. both hiding again. Characteristic type 15 to 60 seconds. This behaviour was seen
during the day and the night. The fish remained
moved few centimeters Dead or anesthetized fishes, offered to the coral, motionless, suddenly a
A and stood motionless The of were consumed, but slowly. large swelling was again. change position
half visible at the colony surface after the fish was took less than a second. On the coral they
moved the interstice pulled inside, and re-expansion of the contracted along or out of it, to a
where tentacles took much longer than with regular position on top of a ridge, they stayed a
little while and then moved on to another prey. (or
the interstice. shows of same) Fig. 7 a sequence
2.2 On the reef, by day positions between the rapid movements.
(2) Turning the head. This behaviour occurred
well Withoutartificial light it was much more difficult by day as as by night.
to distinguish the fish from the coral. Only the (3) Snapping movements, possibly eating, with-
fish's Also fled more out seen eyes were perceptible. they changing position. Only by day.
without rapidly than at night. Very small ones crept be- (4) Changing direction, changing posi-
at intervals of 60 seconds. This be- tween the septs, the bigger ones fled away from tion, 15 to
the colony. Consequently, far less fish were seen haviour occurred by day as well as by night.
than of colour reaction during the day at night. As far as noted, (5) Change as on a congener.
they stayed on Meandrina between 10 and 25 m This was only seen in one tank, at night and in
the late whenever the other fish depth. afternoon, ap-
of less proached to a distance than 5 cm by night
2.3 In the aquarium and less than 10 cm by day. In the other tanks
no interaction was observed, not even if the fishes
For a global analysis the aquarium studies were were at close distance.
divided in time units of 5 minutes fish out of the around per each, (6) Coming tentacles, looking
classed and the behaviour was as active, moderately retreating again (fig. 6). Only at night. The active and inactive. The time spent on each be- tentacles did not react to these movements, that
and the carried havioural category was registered also were out very slowly.
the time spent inside or outside of the colony. (7) Swimming slowly along bottom of an
interstice. Observed at night only. The coral
Inactive behaviour can be described as follows: reacted by tipping the back of the fish with the
the fish stays motionless, except for the gills and end of its tentacles, one after another. It was only
the that the latter often whereafter the tentacle resumed its eyes, move perpetually, a slight touch,
independently of each other. Once in a while the original position. anterior of the dorsal fin down. part moves up or
By day, when displaying this inactive behaviour, Active behaviour includes:
fishes either the with the were on coral, their ( 1 ) Moving short distances or changing direction,
in with less than seconds. belly an interstice between two ridges, or out- intervals of 15 This be- side of it on the bottom, or against the wall of haviour is analogous to (1) and (4) of the moder- the aquarium. At night they stayed between the ately active behaviour, only the frequency is tentacles, usually in an interstice. Except for the higher. Occurs by day as well as by night. BIJDRAGEN TOT DE DIERKUNDE, 50 (1) - 1980 93
A of the in the Characteristic of behaviour. Fig. 7. sequence positions on coral, as seen by day, aquarium. type 94 M. E. BUTTER ET AL. - CORAL/FISH ASSOCIATION
The first (2) Moving distances greater than 5 cm at inter- the beginning of an experiment. obser-
in vals of 0 to 60 seconds. Occurs by day as well as vations of this tank were made the late after-
erratic the of second after time by night. They follow an course across noon the day capture. That
colony, sometimes they leave the colony, stay off most "incidents" were recorded: one fish kept
for In the the other the terri- a while, or return immediately. general chasing away one. Next day
less tories the movements are rapid than the shifts over short were settled, centers about 10 cm apart.
distances the of direction. this time there less A real or changes By was aggression.
( 3 ) Snapping movements together with change of fight never occurred, one fish (always the same
behaviour. darted towards the other that position, foraging Mostly seen during one) one, moved
the but time at Sometimes The fish day, one night. they away immediately. more aggressive most
follow an interstice, biting into the coral tissue, frequently changed colour, alternately becoming
sometimes they swim across the sand bottom, lighter and darker. Change of colour was also
into biting it, or they react to a particle suspended noted as an adaptation to the environment.
in the water, chasing after it.
and seen in one A of the time units each of the (4) Aggression flight. Only tank, survey spent on both at night and during the day, but mainly in behavioural categories is given in tables IV and V.
Table IV
Active, moderately active and inactive behaviour in the aquarium, recorded at 11 a.m.,
5 11 p.m. and active active behaviour; p.m. (+ , behaviour; , moderately —, inactive behaviour).
protocol 1 protocol 2 protocol 3 protocol 4
fish 1 fish 2 fish 1 fish 2 fish 1 fish 2 fish 1 fish 2
+ + O O 0 — O +
+ — + + + — + +
+ O + O O — + +
+ + + + + O + O
O — O O + O + +
O — O O O O O O
protocol 5 protocol 6
fish 1 fish 2 fish 1 fish 2
+ O — —
_L 1
O O
+ O
+ + +
+ + o
+ O O
+ +
O O
protocol 7 protocol 8 protocol 9
fish 1 fish 2 fish 1 fish 2 fish 1 fish 2
— + O —
— —. — + O —
O — — — O —
O — O — + O
O + +
O O + —.
O O
O —
O —
Protocols 1 4 made about and about and to are 11 a.m., protocols 5 6 p.m. protocols
7 to 9 about 11 p.m. BIJDRAGEN TOT DE DIERKUNDE, 50 (1) - 1980 95
Table V respect to the fish might be explained partly by
the fish's behavioural characteristics move- units active and inactive (the Time spent on active, moderately behaviour. One time unit is 5 minutes. ments to induce relaxation of the tentacles), but
it is possible that some chemical qualities of the 11 11 a.m. 5 p.m. p.m. fish's skin are also effective.
studies indicate the active 22 11 6 The aquarium that feeding
moderately active 20 9 15 periods of fish and coral do not coincide; this is inactive 6 12 17 in accordance with the field observations. The
fish's lie in it advantage seems to safe shelter,
be that it eats coral tissue, 2 might possible although A ~tes t the is at x on proportions significant consisted of of stomach contents a variety organ- the 0.005 level: evidently the fishes are more active isms. Whether the coral benefits by this associa- during the day than at night. The time spent on tion is an open question. the from it is in table VI. colony or away given The fish finds protection during the night; there These proportions also differ significantly at the are indications that also during the day it stays 0.005 level. The fishes were always on the colony on or near Meandrina, but field observations are at night, in mid morning 81.4% of the time and as yet too scarce to be conclusive. There is need in the late afternoon 57.1% of the time. for more research, both in the field and in an
experimental environment.
Table VI
outside the coral the in Time spent on or (in aquarium),
time units of minutes. 5 ACKNOWLEDGEMENTS
11 a.m. 5 11 p.m. p.m. We wish to thank Dr. R. P. M. Bak for help and advice,
and Dr. J. S. Stephens, Dr. J. Randall and Dr. J. H. Stock on the coral 39 18 38 for their aid in the identification of the fish. The Carmabi outside the coral 9 14 0 provided laboratory accomodation and diving facilities. For
diving assistance Mr. F. Isabella, Mr. O. Frans and Mr. A.
Tiel are acknowledged.
CONCLUSION
REFERENCES
There is a clear commensal relation between the
ALLEN, G. R., 1975. The anemone fishes, their classifica- fish, Emblemariopsis diaphana, and the coral, tion and biology (2nd ed.): 1-352 (T. F. H. Publica- Meandrina meandrites other coral (occasionally tions Inc. Ltd., Hong Kong). Even in Santa Marta where ALBRECHT, species). (Colombia), H., 1977. Einige Beobachtungen an Anemonen- fische in der Karibischen See. Bijdr. Dierk., 47 (1): Meandrina is rare, the fish seemed to be asso- 109-119. ciated with this coral The particular species. BUTTER, M. E., 1979. Biology and infestation rate of Coral-
coral much less the behaves aggressive to fish than lonoxia longicauda, an endoparasitic copepod of the
West Indian reef coral Meandrina other the is meandrites. Bijdr. to organisms, reason why not yet Dierk., 48 (2): 141-155. understood. the adult Although fish may be too MARISCAI,, R., 1966. The symbiosis between tropical sea
for the the fact remains that anemones and fishes: a large a prey coral, review. In: R. I. BOWMAN (ed.), The Galapagos: 157-171 (Berkeley Univ. Press, Berke- it is not attacked and that small individuals are ley). also left alone. when the coral is Only catching STEPHENS, J. S. Jr., 1963. A revised classification of the
close the it evades the blennioid fishes of prey very to fish, snatching the American family Chaenopsidae. Univ. Calif. Pubis. Zool., 68: tentacles. 1-133, pis. I-XV.
1970. Seven new blennies , chaenopsid from the The less aggressive behaviour of the coral with western Atlantic. Copeia, 1970 (2): 280-309.
Received: 13 February 1980