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First published online December 14, 2006
Journal of Experimental Biology 210, 91-96 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.02627
Chemical versus mechanical bioerosion of coral reefs by boring sponges - lessons from Pione cf. vastifica
1 Department of Zoology, Tel Aviv University, Tel Aviv 69978,
Israel
2 Institute of Earth Sciences, The Hebrew University of Jerusalem, Jerusalem
91904, Israel
Author for correspondence (e-mail:
milan{at}post.tau.ac.il)
Accepted 31 October 2006
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Summary |
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 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
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Key words: Porifera, excavation, coral reef, dissolution, Clionaidae
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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). The agents of
destruction are biological, physical and chemical, and in many cases their
effect on the erosion is synergistic
(Hutchings, 1986). Biological
erosion (bioerosion) as a general term refers to the destruction and removal
of consolidated minerals of lithic substrate by the direct action of organisms
(Neumann, 1966). The most
common agents of bioerosion are fish (Risk
and Sammarco, 1982), sea urchins
(Mokady et al., 1996), algae
(Kobluk and Risk, 1977),
molluscs (Londono-Cruz et al.,
2003; Hutchings et al.,
2005), polychaetes and sipunculids
(Lo-Cruz et al., 2003) and
sponges (Holmes et al., 2000;
Hutchings et al., 2005).
Physical erosion is caused by wave movement, storms, etc. Chemical erosion
involves dissolution of the CaCO3 framework and is mainly mediated
by biological activity, either by metabolic acid production or by excretion of
ligands and enzymes. The organisms may also contribute to the erosion through
their physical boring and scraping activity on the substrate.
Boring sponges, mostly from the family Clionaidae, generally dominate the
bioeroder community (Risk et al.,
1995; Calcinai et al.,
2000). Whereas many sponges are chemically or mechanically
defended, some that have no such defenses may have the competitive advantage
of using a substrate that other organisms cannot use. One such strategy is to
bore into the carbonate substrate that is out of reach of most predators, with
the additional advantage of using a space unavailable to their competitors.
The activity of boring sponges has farreaching ecological and economic
effects: they can host many organisms inside their water channels; affect
settlement of new organisms by changing availability of reef areas; shape the
morphology and affect the strength of the reef framework
(Risk and Muller, 1983;
Neumann, 1966); influence the
alkalinity and the dissolved silica of reef-water chemistry; infect cultured
clam, oyster, or abalone populations in marine farms
(Rosell et al., 1999;
Fromont et al., 2005); and bore
into the structure of piers and water breakers
(Warburton, 1958). Boring
sponges have been used for paleoenvironmental reconstruction, for example, by
measuring the size of bore holes in reefs from the geological record
(Edinger and Risk, 1996).
Boring sponges have developed a unique cellular means of penetrating the
substrate (see Bergquist, 1978;
Pomponi, 1980). The sponge
attaches itself onto the substrate and then penetrates by using etching cells
to separate CaCO3 chips from the substrate (size range, 15-85
µm). Chip production constitutes the so-called `mechanical boring' of
sponges; however, detachment of chips from the hard substrate requires the use
of `chemical boring' as well. A groove is chemically etched, isolating a chip
from the substrate. It is then mechanically transferred out of the sponge body
via the water channels.
Rates of bioerosion depend on several biotic and abiotic factors, including
nutrient and food availability, temperature
(Risk et al., 1995;
Hill, 1996;
Holmes et al., 2000),
physiological state of the organism
(Rützler, 1975) and the
density and type of substrate in which the organism bores
(Hutchings, 1986).
The sponge Pione vastifica (Hancock 1849) has a cosmopolitan
distribution (Warburton,
1958). There is evidence for its distribution in west and east
Mediterranean (Bromely et al.,
1990; Rosell and Uriz,
2002), Barbados (Holmes,
2000), the Red Sea, Mozambique and the Seychelles
(Calcinai et al., 2000).
Because of its worldwide distribution, there has been a genuine misconception
regarding its true definition
(Rützler and Stone,
1986), and recently it has been relocated to the genus
Pione within the family Clionaidae
(Rosell and Uriz, 1997). The
sponge hosts many symbiotic organisms, such as zooxanthellae (dinoflagellates)
and Polydorella smurovi (Tzetlin and Britayev, 1985) (Polychaeta),
that live inside its tissue or on its surface, respectively. Despite its high
abundance and distribution over a wide depth range on Red Sea reefs, the
bioerosion activity of P. cf. vastifica has never been studied and
quantified.
The aim of the present study was to determine the erosional impact of this
sponge on the coral reef as a model for the boring sponge erosion rates. We
used P. cf. vastifica despite its relatively low abundance (as
compared with the abundance of other species of boring sponges) in the studied
reefs because of its encrusting (ß) growth form. This growth form
facilitates measurements of chemical versus mechanical boring
activity (see below), whereas the papillate (
) growth form of another
co-occurring boring species is more complicated for such measurements.
We studied P. cf. vastifica distribution and abundance in the coral reef of Elat, measured its bioerosion rate and determined the relative proportion of chemical versus mechanical boring mechanisms. The sturdiness of this species facilitated the development of our laboratory experiments and analytical methodology. The experimental set-up we developed for the study can also be easily adapted for other sponge species.
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Materials and methods |
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Species abundance was estimated using 10x1 m belt transects
(Loya, 1972). Arbitrarily
placed transects (N=15-20) were performed at depths of: 10, 15, 20,
25 and 30 m. The number of individual sponges and their surface area was
recorded for each belt transect. The surface area of each sponge was estimated
by covering it with an equivalent surface of aluminum foil and converting the
aluminum foil mass (MAl; g) to sponge surface area
(Asponge; cm2) using the calibration curve:
Asponge=227xMAl. Analysis of
variance (ANOVA) and nonparametric a posteriori LSD tests were used to analyze
the results.
Laboratory experiments
Three to five reef rock samples (formerly Porites sp. corals,
15 cm diameter), heavily inhabited by Pione cf. vastifica
sponges, were collected from 20 m depth once every three months, and were
placed for a 24 h acclimation period into Plexiglas containers filled with 2.5
l of filtered (0.2 µm) seawater (total N=24). As a control we used
dead coral skeletons (Porites sp. maintained out of the water for
several months), uninfected by any boring organism, that were immersed in
filtered seawater for 48 h prior to the experiments. Prior to immersion, the
inhabited rocks and the control fragments were gently cleaned with a brush and
washed three times to remove all the epibionts that lived on the substrate and
which could affect the water composition. The experiments started after
replacing the seawater in the Plexiglas containers and lasted for 24 h. During
the experiments the containers were aerated and covered to minimize water
evaporation, which can change water condition and composition.
Determination of chemical boring rate
Rate of chemical boring was determined by measuring changes in total
alkalinity (AT) in the seawater during the experiments.
Total alkalinity of `normal' seawater is defined as
(Stumm and Morgan, 1981):
 | (1) |
which in effect is the number of equivalents of strong acid added to a
seawater sample in order to reach the H2CO3 endpoint. In
our experiments, changes in total alkalinity resulted almost entirely from
precipitation or dissolution of CaCO3
(Lazar and Loya, 1991). The
molar amount of CaCO3 dissolved by the sponge was half of the
observed AT increase in the experimental aquarium. Effects
on total alkalinity other than CaCO3 dissolution or precipitation
may result, for example, from AT decrease due to aerobic
respiration and production of HNO3, and the opposite effect may
result from photosynthesis and NO3- assimilation. In our
experimental system these non-conservative effects on AT
were negligible. AT was measured by potentiometric
titration and by fitting a Gran function. The mass of CaCO3
dissolved by the sponge, M(CaCO3) (in g), was
calculated from the change in total alkalinity [
AT
(eq kg-1)] during the experiment (AT at the end
of the experiment minus AT at the beginning, 24 h
earlier) as follows:
 | (2) |
where 100 is the molecular mass of CaCO3;
Vsw is volume (l) of seawater in the experimental
aquarium; and 
sw is the seawater density (1.028 kg
l-1).
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), and Cliona varians (Duchassaing and Michelotti
1864) boring rate was correlated with zooxanthellae abundance and light
irradiance (Hill, 1996).
Determination of mechanical boring rate
At the end of each experiment the aquarium was stirred, the
CaCO3 chips produced by the sponge and settled on the bottom were
resuspended and the seawater was filtered through a glass fiber filter (3
µm) to collect all the chips. The filter with the chips was combusted at
450°C for 6 h to remove all organic matter. After cooling, the residues
were passed through 200 µm and 100 µm sieves, removing large particles,
assuming that the sponge-produced chips lie within a smaller fraction <100
µm (see above). The filtered chips were cooled to -70°C, freezedried to
remove any traces of water and weighed.
Electron microscopy
Small fragments (2x3x3 mm) of rocks containing sponges
were gently broken using sharp knives as chisels. The samples were immersed
for 24 h in diluted sodium hypochlorite. The clean fragments were rinsed three
times for 30 min in distilled water and then three times for 30 min in ethanol
(100%). The samples were then air dried and glued on stubs for examination
with a scanning electron microscope. The fragments were critical-point dried
and sputtered with gold. The preparations were viewed with a JEOL JSM 840A
SEM-microscope (Tokyo, Japan).
Clean sponge spicules for electron microscope examination were obtained by decalcifying sponge samples (immersing the samples overnight in diluted sodium citrate and formic acid) and digesting the tissue (12 h immersion in sodium hypochlorite). The residues were rinsed three times in water and three times in ethanol (100%), mounted on stubs, gold coated and inspected on a JEOL JSM 840A SEM-microscope. The length (N=40) and width (N=25) of complete spicules from each type were measured.
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Results |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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), and
hence the current identification as P. cf. vastifica indicating its
affiliation with this species complex.
Sponge distribution in the reef
In the depth range of this study (down to 30 m depth), the abundance of
P. cf. vastifica increased linearly with depth by 2 individuals
per 10 m2 per 10 m depth (Fig.
2). This finding was corroborated by an ANOVA test, which showed a
significant difference in abundance between the various depths
(P<0.001), and an a-posteriori test, which revealed three
main depth-related abundance groups (10, 15 and 20, and 25 and 30 m) in which
the abundance increased with depth.
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Sponge mechanical bioerosion
Electron microscope examination of the substrate excavated by P. cf.
vastifica showed the smooth erosion scars (length: range 36-97 µm,
mean 59±18 µm; width: range 17-73 µm, mean 40±13 µm;
N=15) to be polygonal to oval (often round) in shape
(Fig. 1). Closer observation
revealed that the excavated pit frequently had a small projection in the
middle (Fig. 1E,F), suggesting
that the entire surrounding of this projection had already been dissolved.
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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;
Steindler et al., 2001). Thus,
the encrusting (ß) growth form and the presence of symbiotic algae do not
fit this species (Rützler,
2002a). Recently, material from another previously recognized
P. cf. vastifica from Western Australia was reassigned to P.
velans (Fromont et al.,
2005). Further systematic treatment of the present species from
the Red Sea, such as a comparison with P. mussae (Keller, 1891), will
reveal its proper assignment. In this paper, however, for lack of strong
counter-characteristics, this species is still called P. cf.
vastifica.
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The scarcity of small individuals in the reef is rather puzzling, especially because individual sponge tissue was found to contain oocytes (A.Z., unpublished). This may suggest a long period with no recruitment prior to the present study or that young individuals grow very fast and after reaching a certain size (>100 cm2) their growth rate slows substantially. Alternatively, it might be that the smaller individuals grew within the substrate and took the encrusting growth form only after reaching a larger size. Since in the present study we concentrated on the encrusting growth form, a situation as described above would have been overlooked.
Sponge bioerosion rates
Many studies have examined boring sponges and their activity because of
their unique and important role in the shaping of hard-bottom environments
(e.g. Rützler and Rieger,
1973; Acker and Risk,
1985; Thomas,
1996). Most of these studies, however, measured total
CaCO3 disappearance and frequently focused on the mechanical boring
rates, i.e. the production of CaCO3 chips, while guessing the
amount of the chemical boring rate
(Warburton, 1958) or
calculating (Rützler and Rieger,
1973) it to be 10-2% of the total bioerosion, respectively. The
present study is the first to simultaneously quantify both the chemical and
mechanical bioerosion rates. The mean amount of CaCO3 that was
chemically removed from the substrate was 260 g m-2 sponge
year-1 (Fig. 4),
which is approximately three times more than that mechanically eroded by the
same sponge over the same period (80 g m-2 sponge
year-1). The chemical and mechanical erosion rates correlate
positively (Fig. 6) with a
chemical/mechanical boring rate ratio of 3, reflecting dissolution of
three volumes of CaCO3 during production of one volume of chips.
Indeed, the pattern of the erosion scars seen in pits with incomplete chip
removal (Fig. 1D-F) indicates
that most of the scar has been chemically dissolved, which has not been
previously noted in any other bioeroding sponge. The total bioerosion rate
(chemical plus mechanical) is 340±170 g m-2 sponge
year-1, which is equivalent to sponge bioerosion per reef area of
68±34 g m-2 year-1. Boring activity during
November was significantly higher than during the rest of the examined months
(Fig. 4). The total erosion of
the reef by this Pione species is estimated to be rather small
compared with clionaids (0.2-23.8 kg m-2 year-1 results
given per sponge surface area and not reef area) and other bioeroders (11-724
g m-2 year-1 for sea urchins) reported from the same
reef and from reefs elsewhere [see Schönberg
(Schönberg, 2002b) and
Mokady et al. (Mokady et al.,
1996), respectively].
The large variability between studies in the measured sponge erosion rates
may stem from: (1) Variability in type and density of the substrate. We used
skeletons of dead Porites sp. coral whereas other studies used other
coral species and much denser bricks of CaCO3 or skeletons of
molluscs, as reviewed, for example, in Schönberg
(Schönberg, 2002b). The
latter study found that the measured CaCO3 erosion per unit volume
increased with substrate density. Substrate type may yield erosion rate
variability of up to six times the values for measurements performed on the
same sponge species in the same locality [see, for example, table 4 in
Schönberg (Schönberg,
2002b)]. (2) Differences in the species of sponges studied
(Schönberg, 2002b). The
present research used only one species, P. cf. vastifica. (3)
Variability in sponge age. All specimens studied in this study were mature
individuals, which bore more slowly, whereas other studies used young sponges
or fragments that bore faster
(Rützler, 1975). (4) The
length of the sponge's water canals. It was shown that the boring activity
decreases when the water canals pass a certain threshold length
(Neumann, 1966). (5)
Variability in nutrient levels. It was argued that high nutrient levels
stimulate boring rate in sponges (Holmes,
2000). The surface water of the northern Gulf of Aqaba, northern
Red Sea, is depleted of nutrients during summer and may contain relatively
high nutrient levels during spring. (6) Variability in water temperature. The
sponge boring activity that might be temperature-dependent
(Rützler, 2002b) is low
in the cooler water of the northern Gulf of Aqaba (sea surface temperature
ranges of between 20°C and 28°C).
The results of this study indicate that the chemical boring rates of P.
cf. vastifica are constant during a diurnal cycle, showing no change
between night and day (Fig. 5).
Light intensity, the daytime net photosynthesis of the symbiotic zooxanthellae
and the night-time net respiration of the sponge were apparently not reflected
by a change in the boring rate of P. cf. vastifica. This finding is
in contrast to the results of an earlier study showing that the boring rates
of the sponge Cliona varians forma varians correlated with
zooxanthellae abundance and light irradiance
(Hill, 1996). However, it was
shown that for the sponge species studied here, P. cf. vastifica, the
zooxanthella abundance did not correlate with light intensity
(Steindler et al., 2001),
supporting the findings of the present study.
In summary, the present study demonstrated the feasibility of
simultaneously measuring chemical and mechanical boring rates. The combined
chemical and mechanical boring rate of the sponge P. cf. vastifica in
the reefs of the northern Gulf of Aqaba was estimated to be 70 g
m-2 year-1, which is 1-2% of the total growth
(calcification) rate on these reefs (Barnes
and Lazar, 1983). The abundance of P. cf. vastifica in
these reefs is much lower than that of other clionaid sponges. Therefore, the
actual role of boring sponges in northern Red Sea reef bioerosion is most
probably much larger than the rate cited above.
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Acknowledgments |
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Footnotes |
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