CORAL REEF PAPER
BULLETIN OF MARINE SCIENCE, 35(1): 72-79, 1984
ECOLOGICAL SUCCESSION OF REEF CAVITY-DWELLERS
(COELOBITES) IN CORAL RUBBLE
Dong Ryong Choi
ABSTRACT
Ecological succession of reef cavity-dwellers (coelobites or cryptic organisms) in interstices
of coral rubble in the Florida Reef Tract was established by the stratigraphic analysis method.
Colonization begins with encrusting foraminifers, boring bivalves and serpulid worms. Most
of the bryozoans and sponges appear next along with solitary bryozoans and non-boring
bivalves. This community development is climaxed by overgrowth ofthe rubble by a tunicate.
Rubble formed by a shipwreck in the shallow reef margin (about 1.5 m of water) showed
that the succession was completed within 3 years. Generally, the earlier colonizers are solitary
in form and have broader tolerance to various environments, but they are taken over by
colonial organisms in the later stages due to competitive superiority of the colonial forms.
In general, succession of colonization on artificial substrates (ballasts) show similar patterns
as on natural substrates (corals) except for the absence of boring fauna and an extraordinary
development of a few pioneering foraminiferal species (Planorbulina spp., Gypsina spp. and
Homolrema rubrum) on artificial substrates.
Ecological succession was clearly observed in coelobite community development. This may
be due to the unique habitat of coelobites, which is relatively free from physical disturbance
and predation.
Extensive development of cavities is a prominent feature of modern reefs.
Cavities provide additional living space, protection from predators and physical
disturbance, and variable illumination for a variety of sessile, vagile and even
burrowing organisms (Ginsburg, 1983). Organisms living in these reef cavities
have been called or referred to as coelobites (Ginsburg and Schroeder, 1973),
cryptic organisms (Jackson et al., 1971), sciaphiles (Laborel and Vacelet, 1958),
or cryptone (Sollas, 1905).
Ecological studies on coelobites have been carried out by several specialists,
notably by a school represented by Jackson (Jackson, 1977a; b; 1979; Jackson
and Winston, 1982; Buss and Jackson, 1979; Palumbi and Jackson, 1982). They
investigated the solitary and colonial animals in natural and artificial cryptic
environments and analyzed competition among coelobites for living spaces and
their recovery from disturbance events. Morphologic variation of Homotrema
rubrum was discussed by Lowenstam (1968) and Rooney (1970), and polychaete
recruitment in the Great Barrier Reef was documented by Hutchings (1981). Logan
(1975) studied the ecology of an articulate brachiopod in Bermuda.
However, no systematic study on the succession of colonization (basically following definitions by Shelford, 1930 and Odum, 1969) of coelobites on natural
substrata has been attempted so far; the relevant studies are those on non-cryptic
organisms on the artificial substrates (Coe, 1932; Coe and Allen, 1937; Hewatt,
1935; Scheer, 1945; Schumacher, 1974; 1977; Osman, 1977; Sutherland and
Karlson, 1977; Field, 1982).
Numerous coelobites dwell in interstices of coral rubble (Choi and Ginsburg,
1981; Choi, 1982; Choi and Ginsburg, 1983). Coral rubble is the most common
substrate in the reef tract and is easily sampled without damaging living corals.
Coral rubble with a mean size of 20 to 30 cm in diameter was collected from 21
stations from the in-shore lagoon to the fore-reef (40 m depth) along the northern
Florida reef tract. Apparently most of the rubble with a diameter of 20 to 30 cm
72
73
CHOI: ECOLOGICAL SUCCESSION OF COELOBITES
Hemet
rema
Bryozoa
3
2
by
Figure I. Method used for reconstruction of succession of colonization. The upper figure shows a
diagrammatic section of the underside of the rubble, and the lower figure shows a reconstructed
succession of colonization. The area shown in vertical lines in the lower figure indicates the time of
non-colonization. This method is commonly used in analysis of stratigraphic sequence in geology.
avoided frequent movements during the storms, which is evidenced by development of coralline algae exclusively on the upper side of rubble. This infrequent
movement may have provided stable interstitial environments enabling coelobites
to grow continuously without major physical interruptions. The samples were
slabbed and analyzed. Restoration of the succession of colonization was established from overgrowth relationships, or stratigraphic analysis method as shown
in Figure 1. The "stratigraphic successional sequence" of coelobites in each piece
of rubble was correlated with the succession seen in all other samples in each
locality (Figs. 2 and 3). Correlation of the numerous successions revealed that
several major organisms regularly colonize cryptic habitats at certain stages and
that others have strong inter- or intra-specific competition and/or seasonal colonization patterns.
RESULTS
The results derived from use of the stratigraphic method are shown in Figure
4. This figure was compiled to show the major colonization stages of each coelobite. From this figure, the following three colonization stages are recognized:
(I) pioneering stage characterized by attachment of pioneering organisms on the
74
BULLETIN OF MARINE SCIENCE, VOL. 35, NO. I, 1984
I~
Terebellid
.-L-LL,
~Barb.
l.J.-L
Step.
cam
I~
~
~e~u~m
Scrupa,~
stage
'111
L1chenopora
II
I
I III
Gastro, ~
~~~~C,a
11
teginopore/la
m~nilTab'
Climax
I
1
f?epta eonell
v;olaceafl
I
CI)
a~
-
Ol
o
f'
I
CII
~
I ~Carpen.
yn·1
~y'opo
~Homo.~
iare
s,- no
<;
2
ma ,..........,
III'~
,...j
I
~s111
Itp
~~~~ft1c
lampa
I I
'Ito' aI<'
Homotremo
n
III
S U
STRATEU
ISLithO
I 'ph0g4
nr
\Gastr
~~
-..
c:
;ona
I
:.!..e ocn< !Sma.....,
I~Hom~
trem~
Ol
<Homo-I~
~tremG
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II)
Til
mODOre a
.•••
Coralline algae
rroli than
::l
<iR-
U
1
c:
W
Pioneering
sta ge
U
Figure 2, Example of succession of colonization restored by the stratigraphic analysis method, showing major stages of colonization in relation to space. This is a composite diagram restored from nine
pieces of coral rubble in the north of Ajax Reef, northern Florida Reef Tract (marginal reef, 1.5 to 5
meters deep), The restoration was made in each sample locality, and synthesized as seen in Figure 4,
I: Time of active growth of colonies or individuals, 2: Time of larval settlement on the substratum,
or start of colonization, 3: Time of non-colonization.
surface of new substrate, (2) encrusting stage shown by strong competition for
available space by invaders, and (3) climax stage, evidenced by scattering immigration of small and weak fauna into still available narrow space and final
overgrowth of the coral rubble by a tunicate.
Rubble formed by a shipwreck shows that the time span of this one cycle is
within 3 years in the shallow reef margin (about 1.5 m of water) of the Florida
reef.
Pioneering Stage, - The first pioneers to colonize the cryptic habitat are represented by solitary organisms: Homotrema rubrum, Planorbu/ina spp., Gypsina
sp., boring bivalves, and serpulid worms. Thalamoporella mayon' (bryozoa), a
high energy environment indicator (Choi and Ginsburg, 1983), appears at the end
of this stage.
Encrusting Stage,-In the encrusting stage, many of the bryozoan species occupy
available territories. The representative bryozoans are Hippopodina feegeensis,
Parellisina latirostris. Rhynchozoon rostratum and Cleidochasma porcellana. Intricate selective overgrowth competition among them was observed in samples
from Florida as has previously been described by Jackson (1979) and Buss and
Jackson (1979) in cryptic habitats from Jamaica reefs. The invasion of sponges
in the late stage is characteristic along with massive colonization of space-con-
75
CHOI: ECOLOGICAL SUCCESSION OF COELOBlTES
SCHOONER
REEF
Climax
stage
CIl
Cl
C
+-
en
S Itg/nopo,.
mognl fob,l.
en
:::J
•...
V
<::
W
Pioneering
sto ge
SUBSTR
Figure 3. Another example of restored succession of colonization in coral rubble of a lagoon reef
(Schooner Reef) of Northern Florida Reef Tract. Five well-colonized coral rubble were chosen for this
restoration. Note the similar pattern of succession as that in marginal reef(north of Ajax Reef) shown
in Figure 2.
suming cheilostomes (Parasmittina Spp., Microporella ciliata, Stylopoma spongites, Exechonella antillea and Celeporaria tubulosa). With the spotty colonization
of several bryozoans (Reptadeonella vio/acea, Trematooecia turrita and Steginoporella magnilabris) at the end of the stage, most of the available space is
occupied.
Climax Stage. - This stage is composed of two substages: (1) the early substage,
characterized by scattered immigration of "solitary" or branching bryozoans
(Lichenopora and Scrupocellaria), non-boring bivalves and a scyphozoa, and (2)
the late substage, characterized by overgrowth of rubble by a tunicate (Didemnum
candidum), which covers all senior inhabitants mainly in illuminated areas and
is accompanied by isolated individuals of Barbatia domingensis (bivalve) in the
less illuminated area (in the central part of the underside of the coral rubble).
Occasionally, a sabellid worm will envelop the piece of rubble at this stage,
covering over every senior resident, induding the tunicate.
DISCUSSION
Ecological features ofthe coelobites in colonization succession are summarized
in Figure 5. Cryptic inhabitants are divided into residents that have only the
overgrowth mechanism for competition (foraminifers, scyphozoans, and bivalves), and those armed with toxins as well as strong overgrowth (sponges and
tunicates; see the summary by Jackson, 1977a).
Colonization begins with the establishment of small attachment bases by for-
76
BULLETIN OF MARINE SCIENCE. VOL. 35. NO. I. 1984
F 0 r m s
Pioneer. Encrusting
stolle
Q)
0
0>
<{
.!. .~
E-
~·c
0
u..
Coel
..
0
Q)
.-~
0
a..
0
0
N
0
>-
..
Q)
borgeseni;
Hydro/it
hon
Mesophyllum
s p.
Neogoniolithon
megocoipum
Peysson nel 110 s p.
Gou/erpa?
s p.
Ijom'ltrema
rubrum
Carpenterla
spp.
Gypsino
s p.
8de IIoidina
sp.
Planorbulin
a sp.
StephanoscYPhu&
s p.
Siphonodictyon
corolliphagum
GUono
cori bbaea
Cliono
vermifero
Cliona
lamp a
CUono vastifica
~/iona
schmidti
cornus
sp.
Spiostrella
sp.
Non-boring
sponge
A
Non-boring
sponge
B
Tha/omoporella
mayor;
Hippo pod; n a fee geensis
ParellAsino
lat;rostr;s
Rhync
ozoon
rostratum
Gleidochosma
porcellana
Para smittin
a
spp.
vi%cea
Repta deone' la
Trematooe
cia
turrita
Steg;noporel/a
magnilabris
Microporella
ciliata
5chizoporello
errata
5 t y /opomasponyites
Exechonello
on illea
Cel/eporor/o
tubuloso
Aconthocella
c/ypeoto
Cribrilada
f/oridana
Smit tlpora
americana
5chizoporello
corn uta
Scrupocellaria
s p p.
Li chen opor a
r a dia to
albirostris
Ce
eporaria
Serpulid
worms
Eunice
sp.
Terebellid
gen.
in de t.
stage
In9
I
2
3
~~imall
ooe
I
2
-
---
--
---
----
--
--
--
I'
I
Q)o
c'O
c'<{0
(.)
In
::3
-0
::E
Proc.
Spiroglyphus
s p.
Lithophaga
n'g r a
LithoPha~o
antillarum
Botu/a
usca
Gastrochaena
hian s
permol!
;s weber;
Ostreo
pjicotula
gibbosa
imbricata
Chama
florida
Barbatio
dom;naensis
Oidamnum
candidum
1---
-
Figure 4. Synthesized succession of colonization of coelobites on natural rubble restored by the
stratigraphic analysis method. Thick line shows major colonization stages.
77
CHOI: ECOLOGICAL SUCCESSION OF COELOBITES
T
Sag
Lessthon
o
m e
36 months
Pioneering
stage
Encrusting
e
CI imax
st
stage
2
Substage
3
Succession
a f
colonization
Area
b
covered
fauna
G ro w
t
h
tor
m
Attachment
E pis
0
di c
Competing
Colonial
Solitar
J--- ColonIal
Poi nt----A
t
in v a sl 0 n
ability
Success ion of fouling
communities
by
Scheer
(1945)
1----
rea
S on
We
a k
-------__
AIgoe--
es
.....
>.
Sponge
S t ron g
_
Bry 0 zo a-------Mytilus
Figure 5. Summary of succession of colonization of coelobites in coral rubble as compared to that
of fouling communities by Scheer (1945).
aminifers and boring bivalves in virgin cryptic habitats. After occupation of most
available spaces by bryozoans and sponges by the end of the second (encrusting)
stage, colonization shifts from colonial to solitary organisms, and colonization by
scyphozoans, fragile bryozoans and non-boring bivalves proceeds into the still
available area. Tunicate invasion occurs after the above stages are completed.
The ecological features of the pioneers in colonization order are most interesting.
The pioneers are Homotrema rubrum, Planorbulina spp. (foraminifera), boring
molluscs, serpulid worms and a bryozoa (Thalamoporella mayon), as well as a
calcareous alga, Hydrolithon. Most ofthese pioneers are solitary colonizers except
for Thalamoporella and Hydrolithon, and commonly characterized by strong
adaptability to varying environments, broad spectrum ofJight intensity and water
turbulence (Choi and Ginsburg, 1983). They are also primary colonizers on artificial substrata in the Caribbean (observation by the author; Martindale, pers.
comm.).
The above described patterns of succession agree with Jackson's (1977a) conclusions that solitary forms which are often poor space competitors are among
the first arrivals on substrates but they are taken over in later stages by colonial
organisms due to competitive superiority of the colonial organisms.
Succession of colonization on artificial substrates (rubble of volcanic rocks and
concrete blocks used for ballasts) shows similar patterns to those seen on natural
78
BULLETIN OF MARINE SCIENCE, VOL. 35, NO. I, 1984
substrates (coral rubble; Fig, 5) except that succession on artificial substrates
commonly lacks boring fauna (bivalves and sponges) and is characterized by
dominant development of few pioneering organisms (mainly Planorbulina spp.,
sometimes Gypsina spp. and Homotrema rubrum). Judging from the age of artificial rubble, the succession appears to reach climax stage after a relatively long
period, although it is impossible to determine the specific time span at present.
The general trend of succession described above is similar to that of marine
fouling communities documented by Scheer (1945) from Newport Harbor, California (Fig. 5). There, the dominant organisms shifted from algae and hydroids
to bryozoans, followed by sponges and culminated by Mytilus. This sequence took
over 20 weeks for completion. Although Osman (1977) failed to recognize clear
successional sequence in epifaunal community development on artificial plates
in Woods Hole, the general pattern of succession described by him shows similarity
to that of coelobites: a barnacle-tube polychaete community was the pioneer,
succeeded by bryozoans (Microporella ciliata, Schizoporella errata, etc.), and culminated by an ascidian tunicate (Didemnum candidum) and sabellid worms (Sabel/aria vulgaris, S. microphthalma).
Ecological succession of the epibenthic community has long been discussed by
many biologists; whether it really occurs or not. Some workers recognized a clear
cut pattern of ecologic succession (Hewatt, 1935; Scheer, 1945; Aleem, 1957;
Haderlie, 1969; Field, 1982), but others have emphasized seasonality and physical
disturbance events (Shelford, 1930; McDougall, 1943; Smith et al., 1950; Osman,
1977; Sutherland, 1974; Sutherland and Karlson, 1977). However, in the community development of coelobites, ecological succession was clearly observed.
This seems to be explained by the unique habitat of coelobites, which is relatively
free from predation and physical disturbance (Jackson, 1977a; Osman, 1977).
Repeated colonization of the same group of species especially in encrusting stages
(Figs. 2 and 4) may be attributed to seasonal colonization, yet this does not disturb
the general trend of succession.
ACKNOWLEDGMENTS
I thank R. N. Ginsburg for his advice and encouragement throughout the study. I also thank C. G.
A. Harrison, B. Lidz and anonymous reviewers of the Bulletin of Marine Science for editorial comments. The study was funded by Industrial Associates of Comparative Sedimentology Laboratory.
Contribution from Rosenstiel School of Marine and Atmospheric Science, University of Miami.
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OFCOELOBITES
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DATEACCEPTED: September 23, 1983.
ADDRESS: Comparative Sedimentology Laboratory, Rosenstiel School of Marine and Atmospheric
Science, University of Miami. Fisher Island Station, Miami Beach. Florida 33139.