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Proceedings of the 11th International Coral Reef Symposium, Ft. Lauderdale, Florida, 7-11 July 2008
Session 19
First evidence of coral bleaching stimulating organic
matter release by reef corals
W. Niggl1,2, M. Glas1,2, C. Laforsch2,3, C. Mayr2, and C. Wild1,2
1) Coral Reef Ecology Work Group (CORE), LMU, 80333 München, Germany
2) GeoBio-Center, LMU München, Richard-Wagner-Str. 10, 80333 München, Germany
3) Department Biology II, LMU München, Großhadenerstr. 2, 82152 Martinsried, Germany
Abstract. Corals continuously release mucoid organic exudates in order to clean their surfaces. Additionally,
recent research highlighted the fact that this coral-derived organic matter acts as energy carrier and particle trap
in the oligotrophic coral reef ecosystem, thus playing an important ecological role for recycling of matter and
conservation of nutrients. Environmental stressors such as air exposure, high sediment loads and turbidity are
known to increase the release of coral-derived organic matter. However although it is a common statement in
the literature, scientific data verifying increased coral-derived organic matter release rates during temperature-
induced bleaching events is lacking. This is critical as coral bleaching is the most extensive coral disease world-
wide, and bleaching-induced changes in organic matter release potentially have far reaching consequences for
reef functioning. In this study, a bleaching event was induced in the laboratory and release of dissolved and
particulate organic carbon (DOC and POC) and nitrogen (PN) by the hermatypic coral Acropora spec. was
quantified. Results show that during a bleaching event coral derived POC and PN release almost doubled
compared to unstressed controls. This is the first experimental evidence that coral bleaching affects coral-
derived organic matter release and potentially ensuing element cycles in tropical reef ecosystems.
Key Words: organic, matter, release, bleaching, stimulating
Introduction
Mucoid organic exudates continuously released by
corals (Meikle et al. 1988) play an important role in
heterotrophic feeding (Duerden 1906, Yonge 1930,
Lewis and Price 1975, Lewis 1977, Sleigh et al. 1988,
Goldberg 2002) as a defence against smothering by
sediment (Schumacher 1977), desiccation (Daumas
and Thomassin 1977, Krupp 1984), physical (Brown
and Bythell 2005) and UVR related (Drollet et al.
1997) damage, pathogens (Ducklow and Mitchell
1979, Rublee et al. 1980, Cooney et al. 2002) or
pollutants (Mitchell and Chet 1975, Neff and
Anderson 1981, Bastidas and Garcia 2004). However,
as mucoid organic exudates can dominate the
suspended particulate matter (Johannes 1967,
Marshall 1968) in reef waters, they are obviously also
major components of the coral reef ecosystem’s
nutrient cycles. Wild et al. (2004a) suggested that
these coral-derived mucoid exudates may function as
energy carrier and particle trap, thereby helping to
conserve essential nutrients in oligotrophic tropical
coral reefs. Astonishingly, although the importance of
coral-derived organic matter for reef ecosystem
functioning is well documented, studies quantifying
release rates in correlation to variations in the key
environmental factors are rare.
During the last decades, the phenomenon of coral
bleaching, i.e. the whitening of corals due to the loss
of their symbiotic algae and/or pigments (Brown
1996), has become more and more evident all over the
world. Mass coral bleaching events, triggered mainly
by increases in water temperature, have affected the
world's coral reefs with increasing frequency and
intensity since the late 1970s (Hoegh-Guldberg 2004).
It is predicted that due to a continued increase in
seawater surface temperature (Bijlsma et al. 1995)
from the year 2030 large scale bleaching events will
occur annually (Coles and Brown 2003), leaving only
a very short recovery period for the affected corals.
Despite the apparent actual threat of coral bleaching
for the survival of coral reefs, no data is available
concerning the associated release rates of coral-
derived organic matter. However, such data is
indispensable in order to allow any prediction
concerning nutrient and energy budgets for future
environmental scenarios in coral reefs. In this
laboratory study, release rates of particulate organic
carbon (POC), particulate nitrogen (PN) and
dissolved organic carbon (DOC) by hermatypic corals
of the genus Acropora during a temperature induced
bleaching event were investigated.
In contrast to the methods of previous studies that
have investigated release rates of organic matter in
relation to varying environmental factors excluding
coral bleaching (Crossland 1987, Riegl and Branch
1995, Wild et al. 2005a), this study distinguished
released coral-derived organic matter (mucoid
exudates and host cells) from algal (zooxanthellae)-
derived organic matter.
Material and Methods
Experimental description
All experiments were conducted in August and
September 2007 in the aquarium facilities of the
Department Biology II of LMU München, Germany.
One coral colony of the genus Acropora was
fragmented three weeks prior to the subsequent
experiment in order to allow healing and regeneration.
After the fragmentation, 10 coral fragments (surface
Area: 72.4 - 126.2 cm²) were fixed on ceramic tiles
(4.6 x 4.6 cm) using conventional coral glue. The
experimental set-up consisted of two aquaria, the
resident aquarium (215 L control aquarium), in which
the fragments were maintained at non-heat-stress
conditions, and a 30 L aquarium (bleaching
aquarium), in which the temperature could be
adjusted using a thermostat (HAAKE E52, Germany).
The temperature in the resident aquarium was
monitored by an ONSET underwater temperature
logger revealing a temperature range between 25.6 °C
and 29.3 °C in diurnal cycles. At the beginning of the
incubation experiments, the coral fragments were
placed in ten 1000 ml beakers filled with ca. 900 ml
of filtered seawater (0.2 µm pore size) from the
control aquarium. Manual transference into the
beakers resulted in an expose to air of less than two
seconds. Five beakers, each with one submersed
colony (C1-C5), were placed in the control aquarium,
thereby being exposed to the same temperature
conditions as prior to the start of the experiment. The
submersed fragments in the remaining five beakers
were placed in the bleaching aquarium and acted as
bleaching samples (B1-B5).
Initial water temperature for the bleaching samples
was adjusted to 27 °C and kept at that temperature for
24 h, which complied with two incubation periods
(one incubation period = 12 h). Introduction of
compressed air ensured sufficient air supply and
water circulation. After 12 h incubation, all coral
colonies (B1-B5, C1-C5) were transferred to
additional 1000 ml beakers filled with ca. 900 ml of
freshly filtered seawater (0.2 µm). The incubation
water of the precedent incubation period (IP) was kept
for further processing as described below. This
procedure was repeated every 12 h. After 24 h at 27
°C (IP 1 and 2), the temperature of the bleaching
aquarium was raised every 12 h to a maximum of 32
°C at IP 7. Temperature was decreased to 29 °C and
27 °C for IP 8 and IP 9, respectively.
The occurrence of bleaching was defined as the
point in time when zooxanthellae release rates of the
bleaching samples were significantly higher than the
release rates of the control samples. The surface areas
of all coral fragments were measured as a reference
parameter using the advanced geometry method
described in Naumann et al. (submitted) and based on
computer tomography reference as described by
Laforsch et al. (2008).
Incubation water processing
The exact volume of the incubation water from all
beakers was determined using a graduate 1000 ml
glass cylinder with an accuracy of ± 20 ml. The
incubation water was then stirred using a glass pipette
and sub-samples (n = 1 for each parameter) were
taken in order to determine the following parameters.
For subsequent DOC measurements, 5 ml of the
incubation water were filtered through 0.2 µm syringe
filters (FP 30/0.2 CA, Schleicher and Schell). The
first 2 ml of the filtrate were discarded, but the
following 3 ml were collected in precombusted brown
glass bottles, which were instantly shock-frozen at -80
°C and kept frozen until analysis. For POM
quantification (particulate organic matter), 50 ml of
the incubation water were extracted and filtered by a
vacuum filtration unit onto precombusted GF/F filters
(Whatman, 25 mm diameter). Filters were dried for at
least 48 h at 40 °C and kept dry until analysis.
Another 50 ml were fixed with 2-3 drops of Lugol’s
solution and stored at room temperature for
subsequent enumeration of zooxanthellae using
counting towers and backlight microscopy at 400-
times magnification (Axioplan, Zeiss Germany).
The remaining incubation water was fixed with
formaldehyde (1 % formaldehyde end concentration)
and stored in the dark at 4 °C until further treatment.
Organic matter analysis
POM analyses were conducted using an Elemental
Analyzer NC 2500 for C- and N determinations
(Carlo Erba, Italy). For calibration of the elemental
content of the samples, two standards, Atropine
(C17H23NO3) and Cyclohexanone-2,4-
dinitrophenylhydrazone (C12H14N4O4) were used.
Obtained POC and PN values equal the total amount
of released particulate organic matter (POMt). In
order to obtain the released amounts of coral-derived
particulate organic matter (POMc) the amount of
released algal-derived organic matter (POMa) was
subtracted from POMt. Consequently coral-derived
organic matter is defined as any organic matter
(mucoid exudates, host cells) released by the corals
except algal cells.
For calculating the amount of released POMa, the
POC and PN contents of a distinct number of
zooxanthellae was determined. Therefore a
zooxanthellae suspension was produced by
centrifugation (6000 g) of 400 ml incubation water
from B2 after IP8. The pellet was resuspended in
filtered seawater and the zooxanthellae concentration
(9330 cells ml-1) was determined (methodology see
above). Dilution series of 0.1, 1.0, 10.0 and 50.0 ml of
this solution were subsequently filtered in triplicates
onto precombusted GF/F filters (Whatman). The
filters were dried at 40 °C for at least 48 h before
POM analysis as described above.
The released amounts of algal derived particulate
organic matter (POMa) was determined by
multiplying released numbers of zooxanthellae by the
respective calculated carbon and nitrogen contents of
a single Symbiodinium cell.
Bacteria abundances for 2 bleaching and 2 control
samples were determined using standard DAPI
coloration and fluorescence microscopy. Assuming a
carbon content of 20 fg C per cell (Lee and Fuhrmann
1987), bacteria in the bleaching samples would
account for 3.1 to 5.2 % of the total recorded C
content. In the control samples, bacteria would
account for 4.0 to 6.0 % respectively. In the light of
these calculations microbial contribution was
considered minor.
Unfortunately, bleaching samples B1, B4 and B5
showed necrosis after IP 7 (12 h at 32 °C). The
incubation water of these fragments was therefore
excluded from all further analyses unless otherwise
stated.
DOC concentrations were determined by high
temperature catalytic combustion (HTCO) using a
Rosemount Dohrmann DC-190 total organic carbon
(TOC) analyser and Potassium hydrogenphtalat as
standard solution. Each sample was acidified by
adding 100 µl of 20 % phosphoric acid and purged for
5 min in order to remove inorganic carbon. The DOC
concentrations of each sample were measured five
times. An outlier test was conducted, and the DOC
concentrations of the remaining sub-samples were
averaged.
Results
Induction of a bleaching event
A bleaching event was induced in the laboratory by
exposing the investigated coral fragments to
temperatures increased by 3 to 5 °C (Fig. 1a).
Zooxanthellae enumeration revealed that from the IP
5 (30 °C) to the IP 9 (27 °C) significantly more (Table
1) zooxanthellae were released by the coral fragments
incubated under elevated temperature compared to the
controls (Fig. 1a).
TPN release [mg N h-1 m-2]
0
1
2
3
4
5
6
control fragments
bleaching fragments
Incubation Period (Temperature °C)
1 (27) 2 (27) 3 (28) 4 (29) 5 (30) 6 (31) 7 (32) 8 (29) 9 (27)
PNc release [mg N h-1 m-2]
0
1
2
3
POCc release [mg C h-1 m-2]
0
5
10
15
20
25 control fragments
bleaching fragments
control fragments
bleaching fragments
TPOC release [mg C h-1 m-2]
0
10
20
30
40
control fragments
bleaching fragments
Zoox. release [cells h-1 cm-2]
0
2000
4000
6000
control fragments
bleaching fragments
Figure 1: Summary of organic matter release rates during artificial
bleaching experiment a) zooxanthellae release b) total POC release
c) total PN release d) coral-derived POC release e) coral derived
PN release.
Release of POCt and PNt
Throughout non-bleaching conditions there was no
significant difference between the controls and the
bleaching samples (Fig. 1b,c). Under bleaching
conditions, from IP 5 (30 °C) until IP 9 (27 °C),
a
b
c
d
e
bleaching samples showed significantly (Table 1)
higher POCt and PNt release rates. During IP 8 (29
°C), bleaching samples exhibited highest POCt and
PNt release rates.
Regarding all bleaching samples (B1-B5), including
those partially necrotic, POCt release rates were also
highest during IP 8 (29 ° C) with release rates of 114
± 75 mg C h-1 m-2 (mean ± SD, n = 5) and 14.0 ± 7.6
mg N h-1 m-2 (mean ± SD, n = 5).
Table 1: Summary of statistical analysis (independent samples t-
test): given are p values for hypothesis for no differences between
control fragments and bleaching fragments. * p < 0.05; ** p < 0.01;
*** p < 0.001
Release of POMa and POMc
The released amounts of algal derived particulate
organic matter (POMa) directly correlated with the
zooxanthellae release rates, as POMa release was
calculated by multiplying the released numbers of
zooxanthellae with obtained POC and PN content of
0.3 and 0.05 ng cell-1, respectively (linear regression
of zooxanthellae numbers against respective POC
content, R² = 0.999). Consequently, POCa and PNa
release of the bleaching samples was significantly
higher than that of the control samples whenever
bleaching, as defined above, occurred (Table 1).
Algal-derived POC and PN release of the bleaching
samples was lowest at IP 1 (27 °C) and highest during
IP 7 (32 °C). The highest increase of algae-derived
POC/PN release was found during IP 8 (32 °C), when
bleaching samples released 11 to 35 times more
algae-derived POC and PN than the control samples.
POMc was calculated subtracting POMa from POMt.
Throughout non-bleaching conditions there was no
significant difference between the treatments
concerning POCc and PNc release (Fig. 1d,e). Coral-
derived POC release accounted for 76 to 91 % of the
total released POC and coral-derived PN for 68 to 88
% of total released PN under non-bleached
conditions. Bleaching samples during IP 5 (30 °C)
released significantly (Table 1) more POCc and PNc
compared to the controls. During bleaching, coral
derived POC release accounted for 42 to 82 % of
released POCt and coral-derived PN accounted for 38
to 82 % of total released PN. Maximum POCc and
PNc release could be detected during IP 8 (29 °C).
Release of DOC
No significant differences between bleaching and
control samples concerning DOC concentrations
could be found after any incubation period and
treatment.
Discussion
Coral bleaching and organic matter release
Coral bleaching was induced at elevated temperatures
(30 °C – 32 °C), but also occurred when temperature
was decreased to 29 °C and 27 °C at the end of the
experiment. This temporal delay may be explained by
the effect of heat stress, which can lead to the
breakdown of enzymatic pathways in plants and
animals, resulting in metabolic or biochemical
dysfunction (Cossins and Bowler 1987). Reinstalling
these enzymatic pathways may take a few hours to
days, depending on the damage evoked by heat stress.
Thus, although temperatures were adjusted to non-
bleaching conditions, the release rates were still
elevated in the bleaching samples.
Besides the total release of POM, the exclusive
release of particulate coral-derived organic matter was
increased. This may be attributed to either increased
release of mucoid exudates or increased release of
coral cellular material as a consequence of the
bleaching mechanism (e.g. host cell detachment). If
the mechanism of bleaching, i.e. the release of
zooxanthellae, was solely responsible for increased
coral-derived organic matter release, the release of
coral-derived organic matter should be highest when
zooxanthellae release during bleaching was highest.
However, coral-derived organic matter release was
highest at 29 °C when zooxanthellae release had
already decreased (Fig. 1a,d,e). Consequently, the
mechanism of bleaching was very likely not the only
factor responsible for increased coral-derived organic
matter release. Therefore, increased release of mucoid
exudates apparently co-occurred during bleaching.
The measured total organic matter release rates of
the non-stressed control fragments are in the same
range as release rates described in previous field
studies (Table 2). Including coral fragments with
partial necrosis, release rates were similar to those
measured during air exposure (Table 2). As necrosis
is one of five possible mechanisms resulting in
expulsion of zooxanthellae (Gates et al. 1992), and
commonly occurs during bleaching (Glynn et al.
1985), these findings underline the relevance of
bleaching events for energy and nutrient cycles in the
reef ecosystem. This is confirmed by the study of
Wild et al. (2004b), who found that coral-derived
organic matter is rapidly degraded by reef microbes,
in contrast to zooxanthellae-derived organic matter,
which may rather represent a loss of energy and
nutrients for the reef ecosystem (Wild et al. 2005b).
Temp Zoox. TPOC TPN POCa PNa POCc PNc
30 °C *** *** *** *** *** *** ***
31 °C * ** *** * * ** 0.065
32 °C *** ** *** *** *** 0.079 *
29 °C *** *** *** *** *** ** **
27 °C ** ** ** ** ** * 0.115
This study also showed that DOC release was not
influenced by coral bleaching. This is surprising as
Wild et al. (2004a) demonstrated that between 56 and
80 % of coral mucus can dissolve in the surrounding
seawater. However, it is very likely that a high
proportion of the released DOC was re-consumed by
the coral and associated bacteria (Sorokin 1973, Al-
Moghrabi et al. 1993). This explanation is supported
by the studies of Ferrier-Pages et al. (1998) and
Naumann et al. (unpublished data), who found that it
is generally difficult to detect any DOC release by
corals in a closed system such as a beaker.
Furthermore, DOM polymers can spontaneously
assemble to form polymer gels, thus entering the
POM pool (Chin et al. 1998), which could have lead
to a removal of surplus DOC from the incubation
water.
Ecological implications
Increased coral-derived POM release during
bleaching can probably be attributed to increased
release of cellular matter and/or to increased release
of mucoid exudates. Increased release of cellular
matter during bleaching can be explained by the
mechanism of bleaching, which may lead to loss of
parts of or entire coral cells. However, the reason for
increased release of mucoid exudates is harder to
surmise. Up to 45 % of carbon fixed daily by the
zooxanthellae can be released as organic matter by the
host coral (Davies 1984, Crossland 1987, Bythell
1988, Edmunds and Davies 1989). A bleached coral is
in a state of energy shortage as the algal symbionts,
which are capable of providing the coral host with up
to 100 % of its daily metabolic energy requirements
(Muscatine et al. 1981), are lost. Thus, it is not
surprising that coral bleaching can affect the release
rates of organic matter.
However, there are some ecological advantages and
disadvantages of up-regulation of mucoid organic
matter release during coral bleaching. On one hand,
energy loss via mucoid organic matter release may
further reduce the ability of corals to cope with
bleaching, whereas on the other hand mucoid
exudates release may function for heterotrophic
feeding (reviewed by Brown and Bythell 2005),
which could partly compensate the missing
autotrophic contribution to the coral’s energy demand
during bleaching. Further, increased mucoid exudates
release during bleaching may also help to protect the
coral against high UV radiation often associated with
coral bleaching (e. g. Jokiel 1980, Fisk and Done
1985, Gleason and Wellington 1993) as UV-
absorbing substances such as mycosporine-like amino
acids (MAAs) have been detected in coral mucus
(reviewed by Dunlap and Shick 1998).
Coral mucus may play an important role in
providing various defence capabilities against
pathogenic organisms (reviewed by Brown and
Bythell 2005). During bleaching, corals are in a state
of stress owing to energy shortage and damaged
epithelia, and thus are more vulnerable to pathogens
which may occur with increased abundances at
elevated temperatures. Increased mucus release may
be a response to decrease vulnerability and support
defence against pathogens.
Recent research revealed that azoxanthellate cold
water corals release POM in comparable quantities to
zooxanthellate warm water corals (Wild et al. in
press). This indicates that the release of mucoid
exudates by corals is largely decoupled from the
presence of zooxanthellae and thus represents a
general response to any kind of environmental stress,
including bleaching.
Acknowledgements
We thank V. Witt, M. Kredler, F. Mayer, M. Naumann, A. Haas, C.
Jantzen and C. Williamson for assistance during experiments or
subsequent analyses and R. Tollrian for his support of this study,
which was funded by grant Wi 2677/2-1 of the German Research
Foundation (DFG) and a PhD stipend of University of
Bavaria/Bavarian Elite Advancement to W. Niggl.
Reference List
Al-Moghrabi S, Allemand D, Jaubert J (1993) Valine uptake by the
scleractinian coral Galaxea fascicularis characterization and
effect of light and nutritional status. . J Comp Physiol B
163:355-362
Study site Stress Mucus C release
(mg h-1 m-2) Mucus N release
(mg h-1 m-2) N Method Reference
Heron Island Air expos. 117 ± 79 13 ± 8 8 Container Wild et al. 2005
Heron Island No 10 ± 5 1.3 ± 0.8 8 Beaker Wild et al. 2005
Heron Island No 7 ± 3 0.8 ± 0.4 8 Beaker Wild et al. 2005
Eilat No 1.4 - 4.2 Perspex Chamber Crossland 1987
Aqaba No 1.0 - 3.0 0.1 - 0.4 5 Beaker Naumann unpubl.
coral-derived algal-derived coral-derived algal-derived
Laboratory No 7.8 ± 2.1 1.5 ± 0.8 1.1 ± 0.3 0.3 ± 0.1 45 Beaker This study
Laboratory Bleach. 30° 8.6 ± 1.0 1.9 ± 0.5 1.5 ± 0.3 0.3 ± 0.1 5 Beaker This study
Laboratory Bleach. 31° 10.2 ± 1.8 10.1 ± 5.0 1.5 ± 0.5 1.8 ± 0.9 5 Beaker This study
Laboratory Bleach. 32° 11.7 ± 5.0 15.4 ± 2.6 1.7 ± 0.7 2.7 ± 0.5 2 Beaker This study
Laboratory Bleach. 29° 20.4 ± 3.3 14.5 ± 1.0 3.1 ± 0.3 2.6 ± 0.2 2 Beaker This study
Laboratory Bleach. 27° 18.5 ± 9.4 5.9 ± 2.7 2.3 ± 1.0 1.0 ± 0.5 2 Beaker This study
Table 2: Summary of studies examining organic matter release rates by corals of the genus Acropora. In the present study 45 replicates
are displayed, because 5 coral fragments were incubated at 9 different periods. (Note: Previous studies used old definition of mucus and
did not distinguish between coral- and algal-derived organic matter).
Bastidas C, Garcia E (2004) Sublethal effects of mercury and its
distribution in the coral Porites astreoides. Mar Ecol Prog Ser
267:133-143
Bijlsma L, Ehler C, Klein R, Kulshrestha S, McLean R, Mimura N,
Nicholls R, Nurse L, Perez Nieto H, Stakhiv E, Turner R,
Warrick R, (1995) Coastal zones and small islands. In:
Watson RT, Zinyowera MC, Moss RH (eds) Climate change
1995 - Impacts, adaptations and mitigations of climate
change: scientific-technical analyses. IPCC, Cambridge
University Press, New York, USA
Brown B (1996) Coral bleaching: causes and consequences Proc
8th Int Coral Reef Symp, Panama, p 65-74
Brown BE, Bythell JC (2005) Perspectives on mucus secretion in
reef corals. Mar Ecol Prog Ser 296:291-309
Bythell J (1988) A total nitrogen and carbon budget for the elkhorn
coral Acropora palmata (Lamarck). Proc 6th Int Coral Reef
Symp 2:535-540
Chin W, Orellana M, Verdugo P (1998) Spontaneous assembly of
marine dissolved organic matter into polymer gels. Nature
391:568-571
Coles SL, Brown BE (2003) Coral bleaching - Capacity for
acclimatization and adaptation. Adv Mar Biol 46: 183-223
Cooney R, Pantos O, Le Tissier M, Barer M, O’Donnell A, Bythell
J (2002) Characterisation of the bacterial consortium
associated with black band disease in coral using molecular
microbiological techniques. Environ Microbiol 4:401–413
Cossins A, Bowler K (1987) Temperature biology of animals.
Chapman and Hall, London
Crossland C (1987) In situ release of mucus and DOC-lipid from
the coral Acropora variabilis and Stylophora pistillata in
different light regimes. Coral Reefs 6:35-42
Daumas R, Thomassin BA (1977) Protein fractions in coral and
zoantharian mucus: possible evolution in coral reef
environments. Proc 3rd Int Coral Reef Symp 1:517–523
Davies P (1984) The role of zooxanthellae in the nutritional energy
requirements of Pocillopora eydouxi. Coral Reefs:181-186
Drollet JH, Teai T, Faucon M, Martin PMV (1997) Field study of
the compensatory changes in UV-absorbing compounds in the
mucus of the solitary coral (Fungia repada) (Scleractinia:
Fungiidae) in relation to solar UV radiation, seawater
temperature, and other coincident physicochemical
parameters. Mar Freshw Res 48:329-333
Ducklow HW, Mitchell R (1979) Bacterial populations and
adaptations in the mucus layers on living corals. Limnol
Oceanogr 24:715-725
Duerden J (1906) The role of mucus in corals. Q J Microsc Science
49:591-614
Dunlap WC, Shick JM (1998) Ultraviolet radiation-absorbing
mycosporine-like amino acids in coral reef organisms: a
biochemical and environmental perspective. J Phycol 34:418–
430
Edmunds P, Davies P (1989) An energy budget for Porites porites
(Scleractinia), growing in a stressed environment. Coral Reefs
8:37-43
Ferrier-Pages C, Gattuso JP, Cauwet G, Jaubert J, Allemand D
(1998) Release of dissolved organic carbon and nitrogen by
the zooxanthellate coral Galaxea fascicularis. Mar Ecol Progr
Ser 172:265-274
Fisk D, Done T (1985) Taxonomic and bathymetric patterns of
bleaching in corals, Myrmidon Reef (Queensland). Proc 5th
Int Coral Reef Congr 6:149-154
Gates RD, Baghdasarian G, Muscatine L (1992) Temperature
Stress Causes Host-Cell Detachment in Symbiotic Cnidarians
- Implications for Coral Bleaching. Biol Bull 182:324-332
Gleason D, Wellington G (1993) Ultraviolet radiation and coral
bleaching. Nature 365:836-838
Glynn P, Peters E, Muscatine L (1985) Coral tissue microstructure
and necrosis: relation to catastrophic coral mortality in
Panama. Dis aquat Org 1:29-37
Goldberg W (2002) Feeding behaviour, epidermal structure and
mucus cytochemistry of the scleractinian Mycetophyllis reesi,
a coral without tentacles. Tissue Cell 34:232-245
Hoegh-Guldberg O (2004) Coral reefs in a century of rapid
environmental change. Symbiosis 37:1-31
Johannes R (1967) Ecology of organic aggregates in the vicinity of
a coral reef. Limnol Oceanogr 7:189-195
Jokiel PL (1980) Solar Ultraviolet-Radiation and Coral-Reef
Epifauna. Science 207:1069-1071
Krupp DA (1984) Mucus production by corals exposed during an
extreme low tide. Pac Sci 38:1-11
Laforsch C, Christoph E, Glaser C, Naumann M, Niggl W (2008) A
precise and non-destructive method to calculate the surface
area in living scleractinian corals using X-ray computed
tomography and 3D modeling. Coral Reefs [doi:
10.1007/s00338-008-0405-4]
Lee S, Fuhrmann JA (1987) Relationships between Biovolume and
Biomass of Naturally Derived Marine Bacterioplankton.
Applied And Environmental Microbiology 53:1298-1303
Lewis J (1977) Suspension feeding in Atlantic reef corals and the
importance of suspended particulate matter as a food source.
Proc 3rd Int Coral Reef Symp 1:405-408
Lewis J, Price W (1975) Feeding mechanisms and feeding
strategies of Atlantic reef corals. J Zool Lond 176:527-544
Marshall M (1968) Observations on organic aggregates in the
vicinity of coral reefs. Marine Biology 2:50-55
Meikle P, Richards G, Yellowlees D (1988) Structural
investigations on the mucus from six species of coral. Mar
Biol 99:187-193
Mitchell R, Chet I (1975) Bacterial attack of corals in polluted
water. Microb Ecol 2:227-233
Muscatine L, McCloskey L, Marian R (1981) Estimating the daily
contribution of carbon from zooxanthellae to coral animal
respiration. Limnol Oceanogr:601-611
Neff J, Anderson JA (1981) Responses of marine animals to
petroleum and specific petroleum hydrocarbons. Science
Publ, London:117-121
Riegl B, Branch M (1995) Effects of sediment on the energy budget
of four scleractinian and five alcyonacean corals. J Exp Mar
Biol Ecol 186:259-275
Rublee P, Lasker H, Gottfried M, Roman M (1980) Production and
bacterial colonization of mucus from the soft coral Briareum
asbestinum. Bull Mar Sci 30:888-893
Schumacher H (1977) Ability in fungiid corals to overcome
sedimentation Proc 3rd Int Coral Reef Symp, p 503-509
Sleigh M, Blake J, Liron N (1988) The propulsion of mucus by
cilia. Am Rev Resp Dis 137
Sorokin Y (1973) On the feeding of some scleractinian corals with
bacteria and dissolved organic matter. Limnol Oceanogr
18:380-385
Wild C, Huettel M, Klueter A, Kremb S, Rasheed M, Joergensen B
(2004a) Coral mucus functions as an energy carrier and
particle trap in the reef ecosystem. Nature 428:66-70
Wild C, Rasheed M, Jantzen C, Cook P, Struck U, Boetius A
(2005b) Benthic metabolism and degradation of natural
particulate organic matter in carbonate and silicate reef sands
of the Northern Red Sea. Mar Ecol Prog Ser 298:69-87
Wild C, Rasheed M, Werner U, Franke U, Johnstone R, Huettel M
(2004b) Degradation and mineralization of coral mucus in
reef environments. Mar Ecol Prog Ser 267:159-171
Wild C, Woyt H, Huettel M (2005a) Influence of coral mucus on
nutrient fluxes in carbonate sands. Mar Ecol Prog Ser 287:87-
98
Yonge C (1930) Studies on the physiology of corals. 1. Feeding
mechanisms and food. Sci Rep Great Barrier Reef Exp 1:13-
57
