Porifera Research: Biodiversity, Innovation and Sustainability - 2007
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Observations on reef coral undermining by the
Caribbean excavating sponge Cliona delitrix
(Demospongiae, Hadromerida)
Andia Chaves-Fonnegra, Sven Zea(*)
Departamento de Biología and Centro de Estudios en Ciencias del Mar – CECIMAR, Universidad Nacional de Colombia,
INVEMAR, Cerro Punta de Betín, AA 10-16, Santa Marta, Colombia. [email protected], [email protected]
Abstract: Sponges which simultaneously encrust and excavate calcareous substratum are strong space competitors in coral
reefs, actively undermining and displacing live coral tissue. On Caribbean reefs, Cliona delitrix colonizes massive corals,
encrusting, deeply excavating and aggressively killing entire coral heads. To establish the details of the process of colonization,
excavation, undermining and death of corals by this sponge, we carried out observations on sponge-colonized corals at San
Andrés Island (SW Caribbean Colombia), and obtained samples for microscopical observation. As it spreads sideward, C.
delitrix removed the upper few mm of the coral skeleton, maintaining its surface slightly lower than the surrounding coral,
following the curved outline of the coral head. Internal excavation resulted in a solid outer supporting frame and a strongly
eroded lace-like internal network. The outer frame was perforated below inhalant papillae by narrow vertical tunnels and
below the large oscules by wide and deep spaces. A band of dying or dead coral surrounded the sponge. The sponge sent out
a front of tissue using pioneering filaments projecting underneath the coral polyps. Long filaments may surface farther off,
forming new bodies that later fuse. From microscopical observations, physical detachment of polyps was ruled out as the
cause of coral death, because coral tissue displacement occurred before significant erosion of the polypar skeletal support
had taken place. When sponge tissue reached underneath coral tissue, the latter remained healthy when still separated by thin
skeletal barriers, but appeared as debris when barriers were broken. Live sponge and coral tissue could occur in direct contact,
in which case there was accumulation of granulous cells in the coral tissue. We hypothesize that the mechanism of coral death
involves close-range tissue, cell and/or biochemical interactions rather than fluid- or mucus-borne allelochemicals.
Keywords: Cliona delitrix, excavation, corals, colonization, cell-cell interactions, Caribbean reefs.
Introduction
Sessile colonial organisms living on hard substrata often
compete for space by overtopping or directly overgrowing
their neighbors. Takeover of space could be achieved by fast
lateral growth that smothers and kills the overgrown tissue,
but the neighbor’s tissue death could precede or parallel space
takeover through deployment of aggressive appendages at
the boundary and/or release of allelochemical substances
(Jackson and Buss 1975, Suchanek and Green 1981, Lang
and Chornesky 1990). Upright growing organisms with a
limited holdfast area avoid competing for space with more
massive or encrusting ones. Similarly, organisms able to
penetrate and excavate into the substratum limit competition
with organisms dwelling over the surface of the substratum
to those points of their body that are exposed (Jackson 1979,
Woodin and Jackson 1979).
Excavating (burrowing, boring) sponges live in cavities
that they themselves bore into calcium carbonate (corals
and coralline substratum, mollusk shells, polychaete tubes,
calcareous algae) (Goreau and Hartman 1963, Rützler 1975).
Excavation is achieved by both mechanical and chemical
etching and removal of coarse silt-size grains through filopodial
extensions of the basal epithelium cellular membrane (see
Rützler and Rieger 1973, Pomponi 1977). Many species only
expose papillae and oscula through which food and oxygen
are taken and wastes eliminated. However, several species
also encrust the excavated substratum and aggressively
compete for space with corals and other reef organisms. Some
may overgrow live tissue of neighboring organisms (e.g.
Vicente 1978). Others, however, avoiding external defense
mechanisms of their neighbors, bore directly under them,
sending excavating tissue fronts preceded by pioneering
tissue filaments, making neighbors detach, apparently by
eroding their support (Ward and Risk 1977, Schönberg and
Wilkinson 2001, Rützler 2002, López-Victoria et al. 2003,
2006). Some papillated sponges also kill surrounding coral
tissue by releasing mucus presumably laden with allelopatic
compounds (Sullivan et al. 1983, Sullivan and Faulkner
1990).
The encrusting and excavating sponge Cliona delitrix Pang,
1973 (lat. delitrix: a destroyer; Hadromerida: Clionaidae) is
considered one of the most destructive bioeroders in reef
corals. It appears as an encrusting layer of bright scarlet tissue
of closely spaced papillae and interspersed large, high collared
oscules in which deep exhalant canals open (Pang 1973). It
248
penetrates deeply (down to 10-12 cm or more) into the coral
skeleton, filling existing and newly eroded spaces with tissue.
The lateral and vertical expansion of the sponge eventually
leads to the overpowering of entire coral heads, sometimes as
large as 1 m in diameter (Pang 1973, Rose and Risk 1985).
The sponge is often surrounded by a band of dead coral from
where live coral tissue has been eliminated (Pang 1973, Rose
and Risk 1985), but the exact mechanism by which this is
achieved is not known. Cliona delitrix has been reported to
increase in abundance in recent decades, at the expense of
live corals, in various reef areas subjected to nutrient runoff
and organic pollution (Rose and Risk 1985, Ward-Paige et al.
2005, Chaves-Fonnegra et al. in press).
With the aim of obtaining a better understanding how
encrusting excavating sponges in general, and C. delitrix
in particular, confront, erode, and kill reef corals, we
undertook detailed field observations on the sponge and its
host corals at San Andrés Island (SW Caribbean, Colombia),
and histological analyses of samples from the sponge-coral
boundary, to establish: (1) substratum preferences and growth
forms, (2) overall excavation processes and, (3) details on the
undermining and killing of live coral tissue.
Materials and methods
San Andrés (12°32’N, 81°43’W) is an oceanic island of
coralline origin, located in the SW Caribbean and surrounded
by a calcareous platform with a windward barrier reef, a
lagoon with patch reefs, and leeward and windward fore
reef terraces with coral carpets (Díaz et al. 1995, 1996).
Observation and sampling took place throughout the leeward,
western margin of the island. There, individuals of Cliona
delitrix were photographed and observed in detail, noting its
host coral species or substratum (pavement, old dead coral),
surface characteristics, aspect of the zone of interaction with
live coral, etc.
To understand why Cliona delitrix tended to grow at a
slightly deeper level than the surrounding substratum, we made
detailed observations and measured the depth of the sponge at
the boundary step using the butt of a caliper (Fig. 1). To study
excavation patterns, several live sponges were fragmented
with hammer and chisel. By bathing in commercial bleach
remains of dead sponges and small coral heads completely
colonized by a live sponge, intact clean skeletons were
obtained. To obtain a crude estimate of the depth of sponge
excavation inside the coral skeleton, a bicycle steel ray was
forcefully driven perpendicularly through one sponge papilla,
approximately at the center of the sponge (Fig. 1). This was
done only in sponges whose host coral was still alive. The
ray was then retrieved and the depth of penetration measured
with a caliper. The size of the sponge, measured as projected
surface area, was statistically correlated to the depth of the
ray penetration using Pierson’s product-moment correlation
coefficient (Sokal and Rohlf 1981). Surface area was obtained
from digital photos using the Coral Count Point Program with
Excel extension (NCRI-NOVA).
To understand the way in which Cliona delitrix excavates
under live coral tissue, portions of the coral at the sponge
border were detached with hammer and chisel. Structures
were measured with a caliper and sketches of the sections
Fig. 1: Cross-section diagram of a massive coral colonized by
Cliona delitrix, showing how measurements of the difference in
depth between the sponge surface and the surrounding coral skeleton
(step), and the approximate depth of excavation (bicycle ray) were
measured.
were made. Some fragments were fixed for histology in seawater 10% formalin neutralized with methenamine (20 gL-1)
for three days, after which they were stored in 70% ethanol.
In the laboratory samples were trimmed and cut into 2 mm
thick slabs with a petrographic low speed circular diamond
saw (Isomet®, Buehler, Chicago). They were then dehydrated,
stained (acid fucsin and crystal violet), and embedded in
Spurr’s low viscosity resin (ERL 4206, Electron Microscopy
Sciences). Resin blocks were cut in two and each cut section
was glued onto microscope slides using fresh resin. Each
section was then ground in a low speed Polisher/Grinder
(Minimet 1000®, Buehler, Chicago) with diamond-coated
grinding paper of increasingly finer grain (79-9 μm), and
then polished by hand with carburendum 1500 grit paper and
metal polishing paste (for details see Rützler 1974, Willenz
and Pomponi 1996, López-Victoria 2003).
Results
Substratum preferences and growth forms
Most individuals of Cliona delitrix were found growing on
live massive corals or on elevated substratum (old dead coral);
none were colonizing branching or thin foliaceous corals
and only a few were dwelling directly on the flat calcareous
pavement (Fig. 2A, B). There was no mucus on the surface
nor was it produced when the sponge was handled. The few
small sponge individuals seen were always on dead areas of
corals, and consisted generally of an oscule with surrounding
papillae, separated or fused (Fig. 2C); individuals larger
than 3-5 cm always completely encrusted the surface of the
excavated area (Fig. 2D). Sponges had inhalant papillae
throughout their surfaces (Fig. 3A), but often the external
border of a given colony was comprised of a belt of smooth
and level tissue, lacking papillae (Fig. 3B).
General observations on the excavation process
The surface of Cliona delitrix colonies was 0.1 to 1.7 cm
lower than the surrounding substratum (from 164 measuring
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Fig. 2: Underwater photographs of Cliona delitrix. A. On coral Siderastrea siderea. B. On pavement. C. Young individual on dead coral. D.
Small individual growing on coral Siderastrea siderea.
points in 30 sponges), being variable within coral species
(mean±1 standard deviation; Diploria labyrinthiformis
0.5±0.2 cm, n=4; Porites astreoides 0.9±0.8 cm, n=2;
Siderastrea siderea 0.5±0.5 cm, n=24; statistical tests were
not carried out because of low sample sizes of all but one
coral species). The surfaces of the sponges that were found
within about 0.5-1 cm of live coral tissue were only a few mm
deeper than that of the coral (Fig. 2D). At greater distances
the surrounding substratum could be higher, forming a step,
because while the sponge eroded the outer coral skeleton to
about the same elevation, the surrounding live coral (or dead
coral covered by crustose coralline algae) had grown further
upwards (Fig. 3B, C). As the sponge spread, it apparently
carved the wall of the step by undermining its base, often with
tissue fingers and papillae appearing beyond the wall margin
(Fig. 3B; 4A, D). When live coral was at some distance from
the sponge, its new upward growth formed a second step (Fig.
3B). Apart from oscular collars and papillae, the sponge did
not elevate its tissue above the initial level.
A single individual of Cliona delitrix could overtake
and completely encrust a medium size (up to ca. 30-50 cm
in diameter) coral head (Fig. 3D). In larger coral heads the
sponge was frequently characterized by several contiguous
mounds, which we assumed were formerly surviving islands
of coral that grew upward until the sponge covered them (Fig.
3C, E). Fragmentation of a few whole coral colonies revealed
that the sponge could send tissue filaments of about 1 mm in
diameter that would extend into the coral skeleton as far as 10
cm from the main sponge body, surfacing to form new sponge
bodies, which would later fuse with the main body.
From inspection of dead sponges and bleached fragments
we found that just below the dermis of the sponge there
remained a rather solid frame, 3 to 6 mm thick, perforated by
vertical tunnels located below each papilla, and by ample and
deep cavities below oscules (Fig. 3F). Vertical tunnels were
made directly into each coral calyx, eroding continuously
downwards (allowing the insertion of bicycle rays to measure
approximate depth of excavation). Below the frame, the
skeleton was strongly eroded to a lace-like thinner network,
thicker towards the periphery of the sponge, thinner towards
the center, traversed by tunnels of the exhalant canals, which
converged into oscular cavities. The bicycle rays penetrated
250
Fig. 3: Underwater photographs
of Cliona delitrix highlighting: A.
Dying and dead coral strands at the
sponge-coral border, underlined by
sponge excavating tissue filaments.
B. The difference in level between
the sponge surface and its
surrounding substratum, product
of further growth of the coral. A
first step (left arrow) between the
sponge border and the surrounding
dead coral band, and a second
step (right arrow) formed as the
live coral grew upwards further.
C. Another example of the step
between the sponge and the coral,
product of further coral growth, but
in this case the coral finally died
and has been covered by crustose
coralline; the sponge maintains
approximately the same curved
outline of the original level where
it started the excavation. D. An
individual completely colonizing
a medium size (ca. 30 cm) coral
head. E. One individual forming
various contiguous mounds, almost
completely colonizing a large
coral head (ca. 1 m). F. A dying
sponge individual showing the
naked underlying coral skeleton
it had eroded. Notice the rather
intact outer frame perforated at the
calices under papillae, and deeply
eroded areas underneath oscules.
up to 10.1 cm inside sponges that had not yet covered a given
coral head. For these sponges, penetration depth was rather
similar between coral species: Diploria labyrinthiformis,
3.7±1.4 cm, n=3; Montastraea faveolata, 4.7±2.1 cm, n=2;
Porites astreoides, 5.2±1.0 cm; n=2; Siderastrea siderea,
4.7±1.6 cm, n=30 (again, no statistical comparisons were
carried out because of small sample sizes in most corals).
Sponge surface tissue area did not correlate statistically
with depth of bicycle ray penetration in Siderastrea siderea
(r=0.36, p=0.063, n=28). For sponges larger than 25 cm2,
depth of ray penetration varied between 3.5 cm and 6.8 cm,
while in smaller sponges it varied between 2 and 3.5 cm. In S.
siderea colonies of about 30 cm in diameter by 20-25 cm in
height, completely overtaken by C. delitrix, we noticed (but
did not measure) that they were excavated almost to their
base.
Undermining by the sponge vs. coral tissue death
Every Cliona delitrix confronting a live coral, regardless of
its size, was surrounded by a band of dead or dying coral. When
coral tissue was dead, the calices appeared clean (coral tissue
was just removed), or already colonized by turf, frondose or
crustose algae. Often the band of dead coral appeared rasped
by the long-spined urchin Diadema antillarum Philippi
1845, algae being partly removed and coral calices leveled
further. Fish bite marks were rare on the edge of coral tissue
confronting the sponge. In coral tissue close ≤5 mm to the
sponge, 1-2 mm to 1-2 cm-wide unhealthy or dead strips of
coral tissue were sometimes seen spreading radially outwards
from the sponge border (Fig. 3A). Dislodging of coral
tissue with hammer and chisel showed that these affected
coral areas were undermined by shallow excavating sponge
pioneering tissue filaments, apparently involved in coral
251
death. In relatively narrow bands of dead coral (<2.5 cm),
an excavating tissue front 1-3 cm thick advanced 0.5-2 cm
below the surface, often penetrating beyond the edge of live
coral tissue, preceded by tissue filaments, reaching upwards
towards coral polyps or extending horizontally farther ahead
(Fig. 4A, B, C). In wider bands of dead coral, the front of
sponge tissue reached only a few mm beyond the edge of the
sponge, but filaments advanced several cm ahead, sometimes
into live coral (Fig. 4D). Thick tissue bridges extended
beneath adjacent sponge bodies of the same individual (Fig.
4E).
The etching marks characteristic of excavating sponge
erosion were evident in ground and polished sections of
the coral skeletons inhabited by Cliona delitrix, including
the encrusted surface. Beneath live coral tissue, sponge
tissue filaments penetrated through existing skeletal spaces,
expanding them, proceeding upwards through the columellar
space of the calices, breaking through dissepiments, until
reaching the base of the polyp. Throughout the filaments
there were abundant granulous, naturally pigmented goldenbrown cells of varied shapes, 12-15 µm in diameter (Fig.
5), also common in the outer surface tissue and reminiscent
of spherulous cells (see Pang 1973). In several places
healthy sponge and coral tissue were separated by still
Fig. 4: Schematic drawings showing how Cliona delitrix
excavating tissue fronts and pioneering filaments reach out below
live coral (A to D), and how two bodies of the same individual
are connected under the surface (E). The leftover coral skeleton
within the sponge tissue was not drawn.
intact dissepiments or walls. But empty calyx spaces where
the sponge had partially penetrated often contained what
appeared to be dead coral tissue debris. In the few instances
where actual sponge and coral tissue contact was seen, coral
granulous cells accumulated (Fig. 5, pers. comm. by Esther
Peters, July 27 2005).
Discussion
Our observations have confirmed that Cliona delitrix is
a highly aggressive and destructive reef sponge, and added
details about its growth form and how it confronts live coral,
allowing us to formulate hypotheses on the mechanism by
which it kills coral tissue.
The few small, young Cliona delitrix observed were
growing on dead coral substratum, indicating that the
larva, possibly planktonic (see Mariani et al. 2000) settles
preferentially on old dead coral. This behavior has been
described for several excavating sponges (see reviews by
Goreau and Hartman 1963, McKenna 1997, Schönberg and
Wilkinson 2001). But for slightly larger individuals, which
were completely surrounded by live coral tissue, one may
wonder if larval settlement could have occurred directly on
live coral tissue. In fact, Rützler (1971) hypothesized that
252
Fig. 5: Photomicrograph of a
ground and polished section of the
lower part of a live polyp of the
coral Siderastrea siderea, being
undermined by the sponge Cliona
delitrix. It shows the carbonate
calyx skeleton (Sk) and the coral
tissue (C), traversed by a sponge
tissue filament (S, outlined for
clarity). Where the sponge and
coral tissues touch, there is an
accumulation of golden-colored
sponge cells (sg) and coral granular
cells (cg, slightly lighter gray near
the sponge tissue, distinguishable
by color under microscope).
mucus-laden larva of the excavating sponges of the genus
Aka (as Siphonodictyon), which release abundant mucus,
might be able smother and kill live coral polyps, then taking
root and expanding. But C. delitrix does not release mucus,
and recent studies have shown that healthy corals prevent
settlement of other organisms on them (Díaz-Pulido and
McCook 2004), perhaps through the use of allelochemicals
(Fearon and Cameron 1997).
As most other encrusting and excavating sponges, Cliona
delitrix tends to grow at a level slightly lower than the
surrounding substratum (see Acker and Risk 1985, Schönberg
and Wilkinson 2001, Rützler 2002, López-Victoria et al.
2003; but see Vicente 1978 for an exception). Rather than
directly overgrowing the adjacent substratum, the lateral
undermining by these sponges tends to remove its upper layer
(elevated septa in corals, crustose and turf algae in fouled
substratum). Differences in height between C. delitrix and
the surrounding substratum were quite variable within a coral
species, showing that other factors apart from the density and
texture of the outer skeleton play a role. By biting the edge of
the live coral that confronts other encrusting and excavating
sponges, corallivorous fish may sometimes be responsible for
initiating and maintaining the difference (see López-Victoria
et al. 2006). But fish bite marks were rare on coral tissue
confronting C. delitrix in San Andrés. Perhaps grazing of the
band of dead coral by sea urchins play a similar role, but we
could not clearly ascertain this. Overall, for C. delitrix we
believe that two opposing factors are responsible: (1) while
the sponge maintains its curved surface at the same level of
the coral skeleton, upward growth of adjacent coral tissue or of
crustose coralline algae increases the height of the substratum
around it and, (2) rasping of the dead coral area by sea-urchins
decreases the height of dead coral areas. Further shrinkage
of the substratum under the live sponge by bioerosion and
subsequent lowering of the sponge surface may also occur
(Acker and Risk 1985). Microscopical observations on
shallow excavating species (Rützler 1971, Zea and Weil 2003)
and in C. delitrix (this study) revealed characteristic etching
marks on the surface of the external skeleton, showing that
some vertical reduction of the substrate level indeed occurs.
However, significant substratum shrinking is unlikely to exist
in the case of C. delitrix, because its outer skeletal frame
remains uniformly thick throughout the sponge. Further
substratum shrinkage would occur only if directly eaten
and scoured by fish or urchins, which does not seem to be
happening, or from mechanical abrasion during storms. In
fact, marked individuals and fragments of shallow excavating
sponges did not shrink within 1 to 5 years of observation
(López-Victoria el al. 2003, S.Z. pers. observations 2005).
The curved surface of Cliona delitrix may be maintained
as it grows, when the lateral erosion and advance is made
preferentially following the same coral skeletal growth
bands, which are laid cyclically in different densities in
various coral species (e.g., Macintyre and Smith 1974,
Huston 1985). Unfortunately, from our skeletal fragments
and skeletal sections we could not ascertain whether this was
the case. The extent of vertical penetration of Cliona delitrix
into a coral while the sponge is still spreading does not seem
to be affected by density or texture of the host coral species’
skeleton, and does not increase significantly as the sponge
increases in size. Perhaps it penetrates only deeper once it
has taken over the entire colony. Similar values for vertical
extension of C. delitrix have been reported in other studies
(5 cm, Rose and Risk 1985; 10-12 cm, Pang 1973; vs. 10
cm in our study). Vertical penetrations of the substratum as
deep as 8 cm occur in other species as well: in Pione lampa
253
de Laubenfels 1950 (see Rützler 1974, as Cliona) and in Aka
coralliphaga (Rützler, 1971) (see Glynn 1997).
The outer advancing tissue front of Cliona delitrix in massive
cerioid corals is similar to the “string of beads” morphology
of excavating tissues in non-encrusting excavating sponges
such as Cliona vermifera, in which vertical lobes of tissue
located within coral calices are interconnected by horizontal
excavating filaments of varying diameters; smaller filaments
penetrate through the thecal wall, invading another calyx;
the calyx is then filled with tissue and eroded vertically
and horizontally cutting dissepiments and septae (Ward and
Risk 1977). This may be a general way by which excavating
sponges erode corals, first filling existing spaces and then
eroding walls and obstacles (see review en Schönberg 2003),
subsequently varying widely within and among species in
further erosion of the coral skeleton. The vertical component
of calix erosion is emphasized in C. delitrix in comparison to
other shallow excavating encrusting sponges.
When they become large enough, some excavating sponge
species add tissue and supporting siliceous skeleton above the
substratum, becoming massive, and often erode all skeletal
connections to the substratum, becoming free-living, in both
cases conforming what is called a gamma stage (e.g., Topsent
1888, Vosmaer 1933, Rützler 1971, Vicente 1978, Calcinai
et al. 1999). Even shallow encrusting excavating species that
spread horizontally in the upper few cm of substratum slightly
thicken their tissue when they run out of space (López-Victoria
et al. 2003). Owing to its rather soft tissue Cliona delitrix is
perhaps not able to grow further upwards. It may compensate
its lack of upward growth with deep vertical penetration into
the substratum. Its excavation pattern of an outer solid shell
and an inner cavernous core provides enough space for the
tissue and water-circulation system, while giving stability
and support to the sponge.
The growth of Cliona delitrix with far-reaching
ramifications inside the coral skeleton allows it to
simultaneously weaken coral tissue in various portions of the
colony. In a similar way, but from a completely eroded central
chamber filled with tissue, some species of the genus Aka
erode tunnels that reach out to several separated places of the
surface of a coral; further expansion of the outgrowths and
the central chamber ends up taking over the entire coral head
(Rützler 1971). Not penetrating deeply, shallow encrusting
and excavating sponges resort to shallow-lying tissue fronts
and closer-range pioneering filaments that penetrate directly
beneath live tissue coral at their borders (Ward and Risk 1977,
Schönberg and Wilkinson 2001, Schönberg 2001, Rützler
2002, López-Victoria et al. 2003, 2006).
Our histological observations of the zone of interaction
between Cliona delitrix and coral tissues show that coral tissue
death occurs before erosion of the calyces is enough to induce
coral polyp detachment. Indeed, coral tissue and its skeletal
support are so strongly interwoven that polyp detachment
seems hardly possible if the skeleton is not thoroughly
eroded. This purely physical detachment has been assumed
in other works with encrusting and excavating sponges
(e.g., López-Victoria et al. 2003, 2006). Coral death in close
vicinity of C. delitrix could be the consequences of the release
of allelochemicals that can kill coral tissue, and which are
known to be present in its organic extract (Chaves-Fonnegra
et al. 2005). Similar effects have been observed in the fistulate
excavating sponges of the genus Aka (Rützler 1971), and have
been attributed to the release of abundant mucus assumed to
be carrying known allelopathic compounds (Sullivan et al.
1983, Sullivan and Faulkner 1990). The mucus is a medium
that helps spreading and retaining compounds on the surface
of corals, facilitating their entrance into tissue (Hay et al.
1998). However, as C. delitrix does not produce mucus, there
must be some other means, if any, for the deployment of the
potentially harmful substances it produces. Whether they are
exuded directly to the water remains to be determined. At any
rate, our histological observations show healthy sponge and
coral tissues within the coral skeleton just separated by thin
carbonate walls, as well as sites of direct contact where the two
tissues are still alive. This appears to indicate that chemical
substances are not being released into the fluids contained
in the coral skeleton. Moreover, the observed accumulation
of cells in coral tissue in direct contact with sponge tissue
points towards close-range cellular or biochemical processes
involved in coral tissue death, which require further study.
Acknowledgments
This paper is part of the M.Sc. thesis of A.Ch.-F., Marine Biology
Program, Universidad Nacional de Colombia at Instituto de
Investigaciones Marinas y Costeras – INVEMAR. Supported by the
Colombian Science Fund – COLCIENCIAS (grant 110109-13544
to C. Duque and S. Zea), Universidad Nacional de Colombia, and
INVEMAR. We are grateful to M. López-Victoria, E. Peters and J.
Reyes for their help with histological techniques and interpretation,
and to J. C. Márquez, L. Castellanos and Banda Dive Shop for
help during field work. Contribution 979 of INVEMAR and 301
of CECIMAR and the Graduate Program in Marine Biology of
the Universidad Nacional de Colombia, Faculty of Sciences. Two
anonymous reviewers helped greatly to improve the manuscript.
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