Marine Ecology. ISSN 0173-9565
ORIGINAL ARTICLE
Current trends of space occupation by encrusting
excavating sponges on Colombian coral reefs
Mateo López-Victoria1,2 & Sven Zea2
1 Instituto de Investigaciones Marinas y Costeras – INVEMAR, Santiago de Cali, Colombia
2 Universidad Nacional de Colombia (Departamento de Biologı́a) y Centro de Estudios en Ciencias del Mar – CECIMAR, INVEMAR, Cerro Punta
de Betı́n, Santa Marta, Colombia
Keywords
Cliona; competition; coral mortality; coral
reefs; excavating sponges; size distribution.
Correspondence
Sven Zea, Universidad Nacional de Colombia
(Departamento de Biologı́a) y Centro de
Estudios en Ciencias del Mar – CECIMAR,
INVEMAR, Cerro Punta de Betı́n, A.A. 1016,
Santa Marta, Colombia.
E-mail: [email protected]
Accepted: 26 November 2004
doi:10.1111/j.1439-0485.2005.00036.x
Abstract
Some sponges of the genus Cliona (Porifera, Hadromerida, Clionidae) simultaneously excavate and encrust calcareous substratum, competing aggressively for
illuminated space with corals and other organisms. To interpret current trends of
reef space occupation, the patterns of distribution and size of three Caribbean
species were examined at San Andrés Island and Islas del Rosario in Colombia.
While Cliona aprica was ubiquitous, C. caribbaea (¼ C. langae) preferred deep
and protected reef zones, and C. tenuis shallow and wave-exposed settings. In
contrast to the effect on other excavating sponges, chronic exposure to raw sewage did not significantly increase the abundance of the studied sponges. Substratum occupation/availability ratios showed a positive tendency of the sponges
toward certain coral skeletons, and a negative or neutral tendency toward calcareous rock, indicating that establishment may be easier on clean, recently dead
coral than on older, heavily incrusted substratum. High relief generally limits
sponge size to that of the illuminated portions of the substratum. A generally
lower proportion of small individuals than of larger ones indicates currently low
recruitment rates and low subsequent mortality. Successful events of higher
recruitment seem to have occurred for C. tenuis. These are related to the massive
acroporid coral die-off in the early 1980s and to asexual dispersion during
storms, resulting in a current 10% substratum cover. Reefs with high coral mortality were and/or are thus more susceptible to colonization and subsequent space
occupation by these sponges, although relief may prevent space monopolization.
Problem
Sponges are a significant component of coral reefs, their
bottom cover and density often being similar to or higher
than those of stony corals (Rützler 1978; Zea 1993). Among
the various morpho-functional types of reef sponges, those
that excavate the calcium carbonate reef framework play a
key role in the balance between reef accretion and erosion
(reviews in Wilkinson 1983; Glynn 1997). Additionally,
excavating sponges that encrust the substratum are also
strong reef space competitors, aggressively undermining
and displacing live coral tissue (Rützler 1975, 2002; LópezVictoria et al. 2003). Indeed, during the last three decades,
Marine Ecology 26 (2005) 33–41 ª 2005 Blackwell Publishing Ltd
the cover of these sponges has increased considerably, especially at zones suffering massive coral tissue die-off from
disease, bleaching and other causes (Cortés et al. 1984;
Glynn 1997; Williams et al. 1999; Rützler 2002). This has
led some authors to catalog them as a contemporary threat
to coral reefs (Antonius & Ballesteros 1998; Williams et al.
1999). The increase of these and other excavating sponges
has also been related to other factors which are detrimental
to reef corals but are favorable to sponges, such as organic
pollution or temperature increase (Rose & Risk 1985; Holmes 1997, 2000; Rützler 2002).
Cliona aprica Pang, 1973, C. caribbaea Carter, 1882
(¼ C. langae Pang, 1973) and C. tenuis Zea & Weil, 2003,
33
Space occupation by encrusting Cliona
subjects of this study, are three of the encrusting excavating Caribbean sponges whose recent increase in space
occupation and resulting coral tissue mortality have been
reported (Glynn 1997; Rützler 2002; López-Victoria et al.
2003; Zea & Weil 2003; López-Victoria & Zea 2004).
These sponges spread laterally, forming a shallow depression in the substratum, ca. 1–2 cm deep and from a few
centimeters to several meters wide, covered extensively or
completely with dark brown to brown-black tissue; vertical excavation of galleries and chambers, filled with dark
yellow tissue, is limited to the upper 1–2 cm layer of the
substratum. They have associated intracellular zooxanthellae and preferentially inhabit well-illuminated substratum
(Zea & Weil 2003). Their undermining process involves
sending out excavating tissue filaments that erode the skeletal support of the coral polyps (Schönberg & Wilkinson
2001; López-Victoria et al. 2003), which retract or are
sloughed off; the sponge then advances over and below
the freed substratum (López-Victoria et al. 2003). To contribute to the understanding of the processes that have
led to current levels of reef space occupation by these
three species, we evaluated their response in terms of density, cover and size, substratum availability, and the presence and abundance of live corals and other bottom
components. Rates of lateral spread against corals and
other neighbors and the factors that control them have
been (López-Victoria et al. 2003; López-Victoria & Zea
2004) and will be published elsewhere.
López-Victoria & Zea
exhalant (oscular) papillae; these may fuse extensively,
forming an incomplete thin crust which may extend sideward up to about 50 cm in diameter. Oscules are up to
1.9 mm in diameter, encircled sometimes by a grayish rim.
C. caribbaea Carter, 1882 (junior synonym C. langae Pang,
1973) covers completely the excavated substratum with a
thicker (up to 2 mm) amber brown or gray brown tissue.
Size may reach up to 1 m in diameter. Oscules are up to
2.3 mm in diameter, scattered and conspicuous, usually
with a creamy rim. Cliona tenuis Zea & Weil, 2003 encrusts
the entire excavated substratum with a thin veneer of rather
transparent brown tissue, with yellowish, greenish, reddish
or orange shades, through which the underlying excavated
carbonate structures are usually visible. Diameters may
reach 3–5 m. Oscules are small and inconspicuous, up to
1.4 mm in diameter. For detailed descriptions and synonymy and for the general ecology of the three species see Zea
& Weil (2003) and López-Victoria et al. (2003).
2. Study areas
The study was carried out at San Andrés Island and at Islas del Rosario Archipelago, Colombia (Fig. 1). San Andrés is an oceanic island located in the SW Caribbean and
surrounded by an extensive calcareous platform with barrier, terrace and lagoonal reefs (Dı́az et al. 1995). Rosario
is a complex of low islands and cays located directly on
the Colombian continental shelf, surrounded by fringing,
terrace and lagoonal reefs (Dı́az et al. 2000; Cendales
et al. 2002).
Material and Methods
1. Studied sponges
3. Data gathering and analyses
Cliona aprica occurs as fields of closely spaced, small (up to
4 mm in diameter), dark brown to black inhalant and
To establish the general distribution and habitat preference of these sponges, an overall qualitative survey of the
Fig. 1. Map of the study area with sampling
stations. At San Andrés: BB, Bajo Bonito (patch
reef at the base of the shallow leeward terrace,
12–15 m in depth); AN, off the raw sewage
outlet (leeward deep terrace, 12 m); WP, deep
Wildlife (leeward deep terrace, 12–15 m); WS,
shallow Wildlife (leeward shallow terrace, 4–
6 m). At Islas del Rosario: MY, Majayura, CF,
Canal del Francés (both part of the windward
fringing reef, 4–6 m).
34
Marine Ecology 26 (2005) 33–41 ª 2005 Blackwell Publishing Ltd
López-Victoria & Zea
studied areas was carried out, whereby sponge presence
and abundance was recorded, in relation to the degree of
reef development and coral health status. Quantitative
density and cover data of the sponges and other benthic
components were obtained at six stations, four at San
Andrés (for C. aprica and C. caribbaea) and two at Islas
del Rosario (for C. tenuis) (Fig. 1). Cliona tenuis also
occurs at San Andrés, but is restricted to the windward
side, where prevailing strong surge prevented quantifications. Cliona aprica and C. caribbaea are scarce at Islas
del Rosario and were thus not quantified there. As we
intended to evaluate the response of these sponges to the
surrounding coralline environment, the stations were chosen for their relatively high sponge abundances. San Andrés stations were located on the two major topographical
features of the leeward platform, the shallow (2–9 m) and
the deep (10–20) m terraces, two gently sloping, hardground shelves separated by a sand channel. The shallow
terrace consists of low-relief pavement interspersed with
small (usually <50 cm diameter) coral heads; the deep
terrace has a profuse development of massive corals, its
outer edge sloping down to the island drop off (see Dı́az
et al. 2000). Shallow Wildlife station (WS, 4–9 m in
depth) was located on the shallow leeward terrace. Deep
Wildlife (WP) and Aguas Negras (AN) stations were both
located on the deep terrace (10–17 m in depth), but AN,
being located off the major sewage outlet of the island,
has a lower relief and sessile animal cover than WP and is
dominated by calcareous rock (dead coral) covered by
turf algae and fine sediments. Bajo Bonito (BB, 9–12 m
in depth) station is a mound-shaped patch reef of large
(up to 2–3 m diameter) coral heads located at the base of
the shallow terrace. The two stations in Islas del Rosario
were located on the windward, north-facing fringing reef,
at the 3–6 m deep elkhorn coral Acropora palmata (now
dead) reef zone. In both stations – Canal del Francés
(CF) and Majayura (MY) – the bottom is covered by
still-standing and fragmented, dead A. palmata, interspersed with large (up to 2–4 m diameter) massive corals.
Sponge density and frequency of occurrence on the various coral skeletons and substrata were recorded in two to
three band transects (20 · 2 m) at each station. A 20-m
tape was deployed on the bottom, and data were obtained
by swimming over a 1-m area on each side of the tape,
using a 1-m-long rod as reference. Every substratum not
occupied by macroinvertebrates or macroalgae, in which
the original builder organism could not be identified (such
as terrace rocky pavement or old dead coral, both heavily
incrusted by turf and/or crustose algae), was combined in
a single category of ‘calcareous rock’. Maximum diameter
of every sponge individual in the band was measured to
the nearest centimeter with a tape measure attached to the
reference rod. Size distribution histograms were drawn for
Marine Ecology 26 (2005) 33–41 ª 2005 Blackwell Publishing Ltd
Space occupation by encrusting Cliona
the following size ranges: 0–5 cm in diameter (small), 6–
15 cm (mid-size), 16–45 cm (large), and >45 cm (very
large); in general, growth is uniform in all directions, with
the exception of very large individuals, which may have
several separated fronts of growth (Acker & Risk 1985).
Cover of sponges, stony corals (live and dead), sand-rubble, other invertebrates, trash, and calcareous rock were
estimated by measuring the distance of the tape that intercepted each component, and calculated as percent area
relative to the total tape length.
The patterns of substratum (coral species or calcareous
rock) utilization by the studied sponges were analyzed by
calculating, for each station (all transects combined), the
ratio of percent sponge individuals occupying a substratum to the percent availability (cover) of that substratum.
This occupation/availability ratio indicates the tendency a
sponge has towards a substratum. If the ratio is >1, the
substratum is occupied in a proportion greater than its
availability; if <1, it is occupied in a proportion lower
than its availability; if the value ¼ 1, it is occupied in the
same proportion of its availability. The ratio is brought
about by processes at larval settlement (choice, avoidance,
or inability to settle) along with differential survival after
settlement, and was used to infer substratum effects in
distribution. For C. aprica and C. caribbaea at San Andrés, using each station as replicate (all transects combined), a Student’s t-test (two tails) was employed to
determine if the occupation/availability ratio was significantly different from 1, with the null hypothesis of mean
ratio ¼ 1, and the alternative hypothesis of mean ratio „
1. The test was carried out only when the sponge–substratum combination was present in three or more stations.
Hence, data for C. tenuis, obtained only at two Islas del
Rosario stations, could not be tested.
Results
1. Distribution, cover and density
Overall, the presence and abundance of the studied excavating sponges was related to depth and degree of wave
exposure, and varied according to the geographical location. At San Andrés, C. aprica was found in almost all
reef zones and at practically all reef depths. In those sites
where hard bottom space seemed limiting, either because
of the high cover of other invertebrates (e.g. corals, sponges) or because there were many macroalgae or trapped
sediments in the light-exposed substratum, this species
grew in semicryptic spaces and in the papillated growth
stage. In contrast, in places where the availability of welllit calcareous rock (as defined in ‘Material and Methods’)
was greater, this species was rather conspicuous; here, it
was encrusting and larger, growing as extensively fused
35
Space occupation by encrusting Cliona
López-Victoria & Zea
papillae. At Islas del Rosario this species was less conspicuous, found only papillated and in shallow and middepth (down to 12 m) lagoonal environments in rubble
and in the base of branching live corals. At San Andrés,
C. caribbaea was found restricted to depths below 5–6 m
in the leeward side and below 12–15 m in the windward
side; it always inhabited well-lit surfaces of the substratum, with a slight tendency to be more abundant in sites
with greater amounts of calcareous rock. At Islas del Rosario this species was rare, restricted to deep (>20 m) leeward reef zones and growing only in the papillated stage.
Cliona tenuis was present and very conspicuous as large
encrusting sheets in shallow (<6–8 m), well-lit surfaces of
windward settings of both San Andrés and Islas del
Rosario. In the latter area, it was restricted to the pavement and the dead A. palmata thickets and rubble of the
northern, windward fringing reefs and fore-reef terraces.
Within these reefs, wherever massive (live) or foliose (live
or dead) corals were dominant, C. tenuis was less abundant. In leeward settings, it occurred only in the shallow
(2–4 m) rocky shore of San Andrés.
Despite the local differences in predominant growth
stage and occurrence in semicryptic versus exposed substratum, throughout the four quantitative stations at San
Andrés, the cover (0.5–2.0%) and density (0.4–0.7
indiv.Æm)2) of C. aprica were of about the same magnitude, with no particular trend in relation to reef zone or
degree of reef development or health status (Tables 1 and
2). In contrast, C. caribbaea had a lower density and
cover than C. aprica, with the largest (although still low)
density (0.3 indiv.Æm)2) and cover (0.3%) at the deep
terrace station located off the raw sewage outlet (AN)
where the reef is strongly impacted. At Islas del Rosario
stations, the C. tenuis cover varied between 7.6% and
9.5%, while its density varied between 1.3 and 1.8
indiv.Æm)2; the station with the greatest C. tenuis abundance (CF) had the highest cover of calcareous rock
(mostly dead branches of the coral A. palmata) and the
lowest cover of live coral and other organisms (mostly zoanthids and macroalgae) (Tables 1 and 2).
2. Size frequency distribution
At deeper San Andrés stations (WP, AN, BB), regardless
of degree of reef development or health status, C. aprica
occurred in a greater number of mid-size (6–15 cm) and
sometimes large (16–45 cm) than of small (0–5 cm) and
very large (>45 cm) individuals (Fig. 2). The same held
true for C. caribbaea at the station off the raw sewage
outlet (AN; the other stations had too few individuals to
express a pattern). On the shallow terrace (WS), C. aprica
had a similar number of small, mid-size and large and a
few very large individuals (there was a single, very large
individual of C. caribbaea at this station). Most individuals of C. aprica at this station were growing on coral
heads, and the few very large ones usually occurred
directly on the terrace flat pavement.
The size frequency of C. tenuis at both Islas del Rosario
stations differed from the other two sponge species at San
Andrés, with a dominance of large individuals and an
important proportion of very large ones. Despite slight
differences in the proportion of bottom components
between the two studied stations, the sponge size distributions were similar (Fig. 2).
3. Substratum utilization
At San Andrés, C. aprica significantly tended to occupy
Siderastrea siderea as substratum in a greater proportion
than its availability (Table 3; ratio ¼ 4.76, P ¼ 0.0006,
Student’s t-test, null hypothesis of ratio ¼ 1, n ¼ 3 stations). The same sponge species had a borderline tendency (ratio ¼ 0.6, P ¼ 0.048, n ¼ 4 stations) to occupy
calcareous rock in a lower proportion than its availability.
Table 1. Percent cover of substratum categories (mean ± 1 SE, of n ¼ 2–3 transects per station).
cover
station
San Andrés
WP (n ¼ 3)
WS (n ¼ 3)
BB (n ¼ 3)
AN (n ¼ 2)
I. del Rosario
CF (n ¼ 3)
MY (n ¼ 3)
cro
44.2
70.2
56.7
76.8
lco
±
±
±
±
2.5
6.0
4.1
1.3
68.9 ± 3.0
45.7 ± 4.9
29.0
20.9
36.7
2.1
snd
±
±
±
±
3.1
1.4
5.3
1.1
13.5 ± 2.6
17.3 ± 1.7
22.7
5.5
3.2
14.1
other
±
±
±
±
2.0
5.2
0.7
0.4
2.3 ± 2.3
6.5 ± 1.3
3.6
1.7
1.4
5.2
±
±
±
±
0.3
0.9
1.1
1.0
6.1 ± 2.5
22.8 ± 5.0
Cliona aprica
Cliona caribbaea
Cliona tenuis
0.5
1.7
2.0
1.5
+
+
+
0.3 ± 0.02
n.p.
n.p.
n.p.
n.p.
n.p.
n.p.
9.5 ± 3.5
7.6 ± 2.3
n.p.
n.p.
±
±
±
±
0.3
1.0
0.7
1.3
Station codes are those of Fig. 1.
cro, calcareous rock (pavement and dead coral strongly incrusted by crustose coralline and turf algae); lco, live coral; snd, sand and rubble; other,
invertebrates, frondose algae, trash; +, present on station but not on transect; n.p., not present.
36
Marine Ecology 26 (2005) 33–41 ª 2005 Blackwell Publishing Ltd
López-Victoria & Zea
Space occupation by encrusting Cliona
Table 2. Density of the studied sponges (mean ± 1 SE, of n ¼ 2–3
transects per station).
density (indiv.Æm)2)
station
San Andrés
WP (n ¼ 3)
WS (n ¼ 3)
BB (n ¼ 3)
AN (n ¼ 2)
I. del Rosario
CF (n ¼ 3)
MY (n ¼ 3)
Cliona aprica
Cliona caribbaea
Cliona tenuis
0.65
0.53
0.55
0.43
0.06
0.01
0.01
0.30
n.p.
n.p.
n.p.
n.p.
±
±
±
±
0.14
0.04
0.12
0.08
n.p.
n.p.
±
±
±
±
0.02
0.01
0.01
0.10
n.p.
n.p.
1.79 ± 0.67
1.33 ± 0.33
Station codes are those of Fig. 1.
n.p., not present.
In contrast, C. caribbaea was found in calcareous rock in
the same proportion as its availability (ratio ¼ 1.1, P ¼
0.31, n ¼ 4 stations). Several other sponge–substratum
combinations exhibited ratios consistently >1, but they
were not significantly different from 1 due to the low
number of replicates. Such was the case for C. aprica and
Agaricia agaricites (mean ratio ¼ 9.0, P ¼ 0.28, n ¼ 3),
and for the same sponge and Montastraea annularis
(ratio ¼ 2.4, P ¼ 0.26, n ¼ 3). The remaining sponge
species-substratum type combinations (of a total of 26)
were not statistically tested because they occurred in only
one to two stations.
Discussion
Wherever the studied encrusting and excavating sponges
occur, their local abundance seems to be controlled,
among other things, by the availability of substratum to
settle and grow, i.e. well-lit calcareous rock (dead coral,
pavement) not overgrown by other macroorganisms.
This appears to be a general trend for zooxanthellate
excavating sponges (see review in Wilkinson 1983). The
Fig. 2. Size-frequency distribution for the
three studied sponges. Size is maximum
diameter. Size intervals are small (0–5 cm),
mid-size (6–15 cm), large (16–45 cm) and very
large (>45 cm). For station codes see Fig. 1.
Table 3. Ratios of substratum occupation/
availability for the studied sponges.
Cliona aprica
substratum (skeleton)
n
ratio
Agaricia agaricites
Montastraea annularis
Porites astreoides
Siderastrea siderea
calcareous rock
3
3
3
3
4
9.0
2.4
2.0
4.8
0.6
±
±
±
±
±
Cliona caribbaea
P
4.7
0.9
0.6
0.3
0.1
(2.5–19.8)
(1.4–4.3)
(0.8–2.9)
(4.2–5.3)
(0.4–1.0)
0.28
0.26
0.25
0.007
0.048
n
ratio
P
4
n.p.
n.p.
+
n.p.
1.1 ± 0.1 (0.9–1.4)
0.32
Values are mean ± 1 SE (minimum-maximum) from n stations where the sponge–substratum
combination was quantified (only those with n ¼ 3 are included). P values are the probability of
a two-tailed Student’s t-test under the null hypothesis of ratio ¼ 1. Sponge–substratum combinations in bold had a ratio significantly different from 1 (P < 0.05).
+, sponge–substratum combination present on transects, but on the 3 stations; n.p., sponge–
substratum combination not present on transects.
Marine Ecology 26 (2005) 33–41 ª 2005 Blackwell Publishing Ltd
37
Space occupation by encrusting Cliona
abundance of C. aprica, however, may be less dependent
on overall substratum availability: what varies is the
small-scale localization (cryptic versus light-exposed) and
the type of growth (papillated versus encrusting).
In some reef areas there has been an increasing abundance of certain clionid sponges near sources of domestic
waste (Rose & Risk 1985; Holmes 1997, 2000; Rützler
2002). Although values were not very high, C. caribbaea
had its greatest densities and cover in the station off the
San Andrés’ raw sewage outlet, in correlation with the
greater amount of available calcareous rock (mostly dead
coral covered by turf algae and fine sediments). The chronic effect of raw sewage has produced extensive coral
death at this site (see Dı́az et al. 1995); here, total excavating sponge cover is of the same magnitude as the live
coral cover (around 2%). The feeding habit of sponges,
which rely heavily on suspended particulate organic matter (e.g. Simpson 1984; Pile 1999), would favor sponges
over corals (see also Zea 1994; Parra-Velandia & Zea
2003; Valderrama & Zea 2003, and references therein).
Nonetheless, the cover and density of encrusting excavating sponges at this site was lower than at other studied
sites in which coral mortality was also important,
although not as high. Perhaps these sponges rely more
heavily on the translocation of photosynthates from their
endosymbiotic zooxanthellae (e.g. Rützler 1990; Rosell &
Uriz 1992), and the turbidity associated with sites close to
sources of runoff limits photosynthesis. Additionally, the
studied sponges spread laterally at lower rates in calcareous rock heavily incrusted by crustose and turf algae
than against live coral tissue (López-Victoria 2003). This
type of substratum, when heavily silted as is the case off
the raw sewage outlet at San Andrés, may also inhibit larval recruitment. Cliona caribbaea can apparently better
cope with these stressful circumstances than C. aprica.
This is reflected in its tendency to occupy heavily
incrusted calcareous rock in the same proportion as its
availability (occupation/availability ratio of 1.1), as
opposed to the tendency to avoid it by C. aprica (occupation/availability ratio of 0.6, borderline significance).
The high cover and abundance of C. tenuis at the fore
reef of the northern fringing reefs of Islas del Rosario parallel the findings of other studies in which its increased
abundance was related to high levels of coral mortality
(Cortés et al. 1984; Glynn 1997; Williams et al. 1999;
Rützler 2002). Islas del Rosario suffered massive die-offs
of acroporid corals during the early 1980s as a consequence of white band disease and other adverse and circumstantial conditions (see Werding & Sánchez 1979;
Ramı́rez 1986; Garzón-Ferreira & Kielman 1993). Today,
the dead A. palmata on the fore front of the windward
fringing reefs is widely covered by C. tenuis. A similarly
high cover of this species was also reported by Williams
38
López-Victoria & Zea
et al. (1999, as C. langae, 10.8%, versus 7.6–9.5% at Islas
del Rosario) in Puerto Rico, where there was also a massive die-off of A. palmata, probably from similar causes
and around the same time. Another case was put forward
by Rützler (2002, as C. caribbaea), who reported cover
values of 1.8–2.3% at the back of the Belizean barrier reef
in 1997; these values increased to 2.7–6.8% after one year,
coinciding with coral mortality associated with stress and
diseases when temperatures were high.
From the few cases in which substratum occupation/
availability ratios could be calculated and statistically tested, there appears to exist a positive tendency, or bias,
towards the occupation of certain coral skeletons (C. aprica) and a negative (C. aprica, borderline significance) or
neutral (C. caribbaea) tendency towards occupying calcareous rock. For these sponges, this ratio could be a measure of substratum suitability, i.e. the combined quality
that a substratum presents for its larvae to attach, and for
the sponge to then excavate and extend laterally. The settlement and subsequent attachment of these sponges is
little known (although see Mariani et al. 2000). Further
growth may then depend on the nature of the underlying
substratum and of the obstacles put forward by live
neighbors (Schönberg 2002; López-Victoria 2003). Our
occupation/availability ratios, however, indicate that it is
more difficult for the studied sponges to settle and/or to
grow in calcareous rock, a heavily incrusted and modified
substratum, than in corals. Since corals are generally able
to prevent direct settlement of other organisms onto their
live tissue (e.g. a Cliona, see McKenna 1997; macroalgae,
see Dı́az-Pulido & McCook 2002), we can assume that
sponges currently living in live coral colonies (in many
cases completely surrounded by live tissue; personal
observation by the authors) must have settled preferentially on rather clean, recently dead tissue areas. This
assumption is supported by the fact that some of these
sponges tend to be more abundant in areas of recent or
ongoing important coral mortalities. In addition, the lateral growth rates of encrusting excavating sponges in calcareous rock are slower than against live coral tissue, and
the latter in turn slower than in clean coral skeletons
(Schönberg & Wilkinson 2001; Schönberg 2002; LópezVictoria 2003).
Maximum size of the studied sponges was limited by
the availability of well-lit substratum. In situations of high
relief, these sponges spread laterally up to a limit given by
the size of the top of the substratum elevations, after
which they thicken their tissue instead (see López-Victoria
et al. 2003). In contrast, in those reefs or terraces with
low relief and with a large cover of calcareous rock unoccupied or only partially occupied by macroalgae or
macroinvertebrates, the sponges were generally much larger. An exception to this pattern was the station off the
Marine Ecology 26 (2005) 33–41 ª 2005 Blackwell Publishing Ltd
López-Victoria & Zea
raw sewage outlet at San Andrés (AN), where the sponges
were not very large, despite an intermediate to low relief
and minimal cover of coral and other macroorganisms.
In this case, as mentioned above, turbidity may limit
growth, aided perhaps by a smothering effect from silt at
the sponge–turf algal border. Another exception was the
shallow Wildlife station, a flat terrace with intermediate
to low relief, where size in C. aprica was evenly distributed among small, mid-size and large individuals. Perhaps lateral growth is limited here because most
individuals of this species are growing on small corals
(<50 cm, mostly Siderastrea siderea). The border between
flat pavement and coral heads is usually overhanging,
making it difficult for the sponges to spread up or down
and grow further. Indeed, in shallow windward settings at
San Andrés, with a greater amount of pavement, this
sponge sometimes reaches very large sizes (authors’ personal observation).
Given that size is not related to age, it is difficult to
infer patterns of recruitment and growth from size frequency distributions. The generally low abundance of
small versus larger individuals, however, indicates that
current recruitment rates to the small size class are relatively low. Moreover, the predominance of larger individuals may also indicate that once a sponge has established,
survival is high and subsequent growth goes generally
unimpeded until the sponge runs out of suitable substratum. In fact, 180 marked individuals of the three studied
sponges seldom lost tissue or died during 13 months of
follow up (López-Victoria 2003). Two scenarios, which
need to be explored by further research, may be producing these size distributions. In the first – under constantly low recruitment rates, low subsequent mortality
and with maximum size limited by available substratum –
new individuals will continually be added to the upper
size classes as they grow. Alternatively – under currently
low but sporadically high recruitment rates, with maximum size also limited by available substratum and perhaps some mortality of large size classes – the larger
individuals would be those that survived the high recruitment events (see also Yoshioka 1998). The latter may be
the case for C. tenuis at Islas del Rosario because the time
of initiation of the local population is known to have
occurred after the massive die-off of Acropora palmata in
the early 1980s (the studied sponges were virtually absent
before; S. Zea, personal observation). Also, about 25% or
perhaps more of the individuals now living in massive
corals apparently colonized them by dispersion from
sponge-colonized dead coral branches moved about during storms (López-Victoria & Zea 2004), in a process of
asexual recruitment. Thus, the current high density and
cover of C. tenuis, and the dominance of large and an
important proportion of very large individuals, can be
Marine Ecology 26 (2005) 33–41 ª 2005 Blackwell Publishing Ltd
Space occupation by encrusting Cliona
ascribed to one or several episodes of above-average
recruitment, which occurred on the reef space newly freed
after the massive death of acroporid corals or after
storms.
From all the above, it seems apparent that reefs which
have had high coral mortalities, or are experiencing lower
but steady coral tissue death, were or continue to be
more susceptible to colonization and subsequent increase
in space occupation by the studied sponges. Complete
reef space monopolization, however, seems unlikely
because relief limits sponge spread.
Conclusions
Local abundance of Cliona aprica, C. caribbaea and C.
tenuis on Colombian Caribbean reefs depends overall on
the availability of well-lit substratum not colonized by
corals and other macroorganisms. In contrast to other
cases, these sponges did not greatly increase their abundance in reefs subjected to chronic organic pollution.
The increase in abundance of C. tenuis in Colombian
Caribbean fore reefs followed the massive die-off of
acroporid corals in the early 1980s. Substratum occupation/availability ratios indicate that establishment may be
more difficult on older substratum than on recently dead
coral. Maximum size is generally limited by the extent
of the illuminated substratum available for lateral
growth. Size frequency distributions point towards currently low recruitment rates and low subsequent mortality. However, haphazard events of higher recruitment,
apparently related to massive coral die-off or asexual dispersion during storms, seem to have occurred for C. tenuis. Coral mortality thus makes reefs more susceptible
to colonization by these sponges, although relief may
prevent space monopolization.
Acknowledgements
This study was supported by the Colombian Science Fund
(COLCIENCIAS, grant 110109-10387), with matching
funds from INVEMAR (Biodiversity and Marine Ecosystems – BEM Program) and Universidad Nacional de
Colombia (National Research Directorship – DINAIN).
Logistic support at Islas del Rosario was provided by R.
Vieira’s CEINER Oceanarium. We are grateful for help
during field work to A. Chaves-Fonnegra, F. Parra-Velandia, L. Banda, B. Ossa, N. Guevara and J. M. Medrano. E.
Weil (University of Puerto Rico) introduced us to the significance of these sponges and accompanied our initial
efforts. The map was made by D. Rozo at INVEMAR’s
GIS–Lab. Contribution 870 of INVEMAR and 249 of CECIMAR and the Graduate Program in Marine Biology of
the Universidad Nacional de Colombia, Faculty of Sciences.
39
Space occupation by encrusting Cliona
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