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First evidence of coral bleaching stimulating organic matter release by reef corals

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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
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
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
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]
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]
POCc release [mg C h-1 m-2]
25 control fragments
bleaching fragments
control fragments
bleaching fragments
TPOC release [mg C h-1 m-2]
control fragments
bleaching fragments
Zoox. release [cells h-1 cm-2]
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),
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
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).
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
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.
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.
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... This is an essential source of naturally-derived nutrients that provides sustenance to coral reef ecosystems (Wild et al., 2004a,b;Wyatt et al., 2013;Mumby & Steneck, 2018;Tanaka & Nakajima, 2018). However, after bleaching events, there can be a short spike in mucus release (Coffroth, 1990;Davey et al., 2008;Fitt et al., 2009;Niggl et al., 2009;Wooldridge, 2009a), and if stressful conditions persist, such as increased sea surface temperatures, mass coral mortality can occur and result in the expulsion of coral tissue from the calcified skeleton (Davey et al., 2008;Leggat et al., 2019). However, there has been very little research into how mass coral mortality events can affect the other organisms on the degraded reef, such as microbial or macroalgal colonisation on the exposed coral skeleton (Diaz-Pulido & McCook 2002;Davey et al. 2008;Haas et al., 2010;Wild et al., 2011) or for how long this natural source of nutrients, driven by anthropogenic events, can persist in local biogeochemical cycles (Rix et al., 2016(Rix et al., , 2017(Rix et al., , 2018Mumby & Steneck, 2018;Deininger & Frigstad, 2019;Radice et al., 2020). ...
... Davey et al. (2008) found that in the weeks that follow coral bleaching, a 30-fold higher production of new nitrogen occurred on coral reefs compared to those that did not experience bleaching. Such nitrogen productivity has also been shown in an experimental setting (Niggl et al., 2009). While release rates of mucusderived POM from corals increase during the early stages of bleaching, providing a burst of nutrients to coral reefs (Coffroth, 1990), these rates can decrease after the initial bleaching response (Fitt et al., 2009;Wooldridge, 2009). ...
... Much of the literature focuses on the mucus released from live corals and how it is recycled within the system (Davey et al., 2008;Naumann et al., 2009;Wild et al., 2004aWild et al., ,b, 2010Wild et al., , 2011, as well as the short term effects of changes in organic matter release after a bleaching event (Niggl et al., 2009;Wooldridge, 2009). Other work such as Radice et al., (2020) supports this by showing that isotopic signatures of particulate organic nitrogen in the water column decreased eight months after a bleaching event. ...
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Anthropogenic nutrient runoff is a major local stressor on coral reefs but compared to research on global climate change and overfishing, progress has been slower at quantifying its effects, particularly at the ecosystem scale. This is due to the difficulties in cost-effectively capturing the high spatio-temporal variability of bioavailable nutrients in reef systems. In this thesis, I examine common bioindicators and associated methodologies for assessing nutrient regimes as well as the relationships between nutrient and biological responses of the bioindicators. I first compare the precision and cost-effectiveness of five nutrient signatures (δ15N, δ13C, %N, %C and C:N Ratio) in a suite of eight indicators across 21 reefs around the inner Seychelles islands. I show that the congruency between the three most precise types (brown macroalgae, green macroalgae and zoanthids) was low, which was likely due to differences in species-specific ecological strategies (e.g. nutrient uptake and/ or storage capacity). I then test the theory that species within the same functional groups should respond similarly to nutrient enrichment using a) passive biomonitoring (sampling along a nutrient gradient) b) active biomonitoring (in situ reciprocal transplant experiment), and c) manipulative laboratory experiments (nutrient supply rates). Overall, these studies suggest that even the responses of morphologically-similar macroalgae with different strategies for nutrient uptake can vary over fine spatio-temporal scales, particularly if they are not nutrient-limited. Finally, I use one of these methodologies in a real-world scenario to investigate the influence of mass coral mortality events on δ15N signatures of transplanted macroalgae 1) before and after the 2016 bleaching event in the Seychelles, and 2) during the 2019 bleaching event in Mo’orea. Both case studies strongly imply that macroalgae can potentially take up this mass release of dead coral tissue, and possibly locking them into local biogeochemical cycles for up to a year after a bleaching event. I conclude that a traits-based approach, using a suite of congruent bioindicators with the same functional traits (i.e. rapid nutrient uptake), would be most cost-effective for future research and monitoring programs.
... In this respect, nearly half of the hard and soft coral cover was lost during the 2016 bleaching event on our study reefs (as previously documented in [Morais et al., 2021a;Tebbett et al., 2022]). Moreover, past research has linked bleaching to the release of organic matter by corals (Niggl et al., 2009) and a recent study linked nitrogen enrichment in macroalgae tissue to a bleaching-driven coral mass mortality event (Vaughan et al., 2021). This Fig. 6. ...
... Given the extent of coral loss at Lizard Island in 2016, and the evidence from past literature that suggests the decay of dead corals releases nutrients (Niggl et al., 2009;Vaughan et al., 2021), it seems reasonable to surmise that a nutrient spike may have occurred. The observed ephemeral nature of the cyanobacterial mats at Lizard Island supports this theory, as nutrients would have been available in a short-lived pulse only as corals died and decayed. ...
Cyanobacterial mats are increasingly recognised as a symptom of coral reef change. However, the spatial distribution of cyanobacterial mats during coral bleaching has received limited attention. We explored cyanobacterial mat distribution during a bleaching event at Lizard Island and considered hydrodynamics as a potential modifier. During bleaching cyanobacterial mats covered up to 34% of the benthos at a transect scale, while some quadrats (1 m²) were covered almost entirely (97.5%). The spatial distribution of cyanobacterial mats was limited to areas with slower water currents. Coral cover declined by 44% overall, although cyanobacterial mats were not spatially coupled to the magnitude of coral loss. Overall, the marked increase in cyanobacterial mat cover was an ephemeral spike, not a sustained change, with cover returning to 0.4% within 6 months. Cyanobacterial mats clearly represent dynamic space holders on coral reefs, with a marked capacity to rapidly exploit change, if conditions are right.
... The deformity index included observed morphological abnormalities such as physical deformities to tentacle buds as well as indicators of larval stress such as open mouths (Agostini et al. 2012) and the presence of mucus (Brown and Bythell 2005;Bosch 2007;Niggl et al. 2009;Bythell and Wild 2011;Wright et al. 2019). In unstressed conditions, coral mouths are open only during feeding, and the gastric cavity functions as a semi-closed system (Agostini et al. 2012). ...
... In unstressed conditions, coral mouths are open only during feeding, and the gastric cavity functions as a semi-closed system (Agostini et al. 2012). Mucus production can be a sign of stress in cnidarians that may be apparent under high-temperature conditions (Brown and Bythell 2005;Bosch 2007;Niggl et al. 2009;Bythell and Wild 2011;Wright et al. 2019). Again, each characteristic was scored separately using SEM images of each sample, and the scores were then added such that a higher score indicated greater deformity. ...
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The Western Antarctic Peninsula is home to a diverse assemblage of deep-sea species and is warming faster than any other region in the Southern Hemisphere. This study investigated how larval development of the Antarctic cold-water coral Flabellum impensum was affected by temperatures consistent with ocean warming trends predicted for the twenty-first century. F. impensum larvae were cultured under four temperature conditions and scanning electron microscopy, transmission electron microscopy, and flow cytometry were used to compare settlement, mortality, larval size, development, deformity, and cellular health over the course of 44 days. While temperature did not impact settlement, mortality, or larval stress, the warmer treatments did have a significant impact on developmental rate. Samples exposed to warmer conditions developed faster than those in cooler conditions. Increased developmental rates were not accompanied by increased stress indicators such as deformity, mortality, or programmed cell death, suggesting that larval health was not negatively impacted by the rate change and may indicate that F. impensum larvae are tolerant of warming temperatures. Development and deformity assessments considered larval condition during the period between release and settlement, when larvae are thought to be especially sensitive to environmental impacts, and when the effects of those impacts on settlement or mortality may be particularly consequential for biogeography and population survival. These results suggest that larval development of F. impensum may be largely resistant to ocean warming trends predicted for the twenty-first century.
... Davey et al. (2008) found that in the weeks that follow coral bleaching, a 30-fold higher production of new nitrogen occurred on coral reefs compared to those that did not experience bleaching. Such nitrogen productivity has also been shown in an experimental setting (Niggl et al. 2009). While release rates of mucusderived POM from corals increase during the early stages of bleaching, providing a burst of nutrients to coral reefs (Coffroth 1990), these rates can decrease after the initial bleaching response (Fitt et al. 2009;Wooldridge 2009). ...
... Connecting letters indicate significant differences between treatments. Stable isotopic signatures were measured in subset samples of the same specimens that were collected from a lownutrient reef (initial), placed in laboratory aquaria to deplete internal nutrient stores for * 7 days (pre-transplant), before they were deployed on the bleached reef for 3 weeks (post-transplant) (n = 10) mucus released from live corals and how it is recycled within the system (Davey et al. 2008;Naumann et al. 2009;Wild et al. 2004aWild et al. , b, 2010Wild et al. , 2011, as well as the short term effects of changes in organic matter release after a bleaching event (Niggl et al. 2009;Wooldridge, 2009). Other work such as Radice et al. (2020) supports this by showing that isotopic signatures of particulate organic nitrogen in the water column decreased 8 months after a bleaching event. ...
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Scleractinian corals are engineers on coral reefs that provide both structural complexity as habitat and sustenance for other reef-associated organisms via the release of organic and inorganic matter. However, coral reefs are facing multiple pressures from climate change and other stressors, which can result in mass coral bleaching and mortality events. Mass mortality of corals results in enhanced release of organic matter, which can cause significant alterations to reef biochemical and recycling processes. There is little known about how long these nutrients are retained within the system, for instance, within the tissues of other benthic organisms. We investigated changes in nitrogen isotopic signatures (δ ¹⁵ N) of macroalgal tissues (a) ~ 1 year after a bleaching event in the Seychelles and (b) ~ 3 months after the peak of a bleaching event in Mo’orea, French Polynesia. In the Seychelles, there was a strong association between absolute loss in both total coral cover and branching coral cover and absolute increase in macroalgal δ ¹⁵ N between 2014 and 2017 (adjusted r ² = 0.79, p = 0.004 and adjusted r ² = 0.86, p = 0.002, respectively). In Mo’orea, a short-term transplant experiment found a significant increase in δ ¹⁵ N in Sargassum mangarevense after specimens were deployed on a reef with high coral mortality for ~ 3 weeks ( p < 0.05). We suggest that coral-derived nutrients can be retained within reef nutrient cycles, and that this can affect other reef-associated organisms over both short- and long-term periods, especially opportunistic species such as macroalgae. These species could therefore proliferate on reefs that have experienced mass mortality events, because they have been provided with both space and nutrient subsidies by the death and decay of corals.
... In corals, sublethal heat stress during summer can compromise primary production and calcification (Reynaud et al. 2003, thereby altering the release of organic and inorganic products (Niggl et al. 2009, Piggot et al. 2009). In contrast, benthic turfand macroalgae may be less sensitive to heat (Koch et al. 2013), showing increased productivity and net growth with rising temperature (Bender et al. 2014). ...
... This contrasts with many reef locations worldwide, where primary production maxima are typically observed during the warmest months of the year (e.g., Scheufen et al. 2017). At the same time, coral-dominated communities displayed enhanced rates of net DOC fluxes with warming (Ea = 0.73 eV), which can be attributed to an increased release of cellular matter and/or mucoid exudates during thermal stress in corals (Niggl et al. 2009, Scheufen et al. 2017. Although mucus released during higher temperatures may help to protect corals against pathogens (Glasl et al. 2016) or high UV radiation (Gleason and Wellington 1993), it poses an increased loss of organic C that can be used for community growth and/or export at constant GPP rates (Fig. 5). ...
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Shifts from coral to algal dominance are expected to increase in tropical coral reefs as a result of anthropogenic disturbances. The consequences for key ecosystem functions such as primary productivity, calcification, and nutrient recycling are poorly understood, particularly under changing environmental conditions. We used a novel in situ incubation approach to compare functions of coral-and algae-dominated communities in the central Red Sea bimonthly over an entire year. In situ gross and net community primary productivity, calcification, dissolved organic carbon fluxes, dissolved inorganic nitrogen fluxes, and their respective activation energies were quantified to describe the effects of seasonal changes. Overall, coral-dominated communities exhibited 30% lower net productivity and 10 times higher calcification than algae-dominated communities. Estimated activation energies indicated a higher thermal sensitivity of coral-dominated communities. In these communities, net productivity and calcification were negatively correlated with temperature (>40% and >65% reduction, respectively, with +5°C increase from winter to summer), while carbon losses via respiration and dissolved organic carbon release were more than doubled at higher temperatures. In contrast, algae-dominated communities doubled net productivity in summer, while calcification and dissolved organic carbon fluxes were unaffected. These results suggest pronounced changes in community functioning associated with phase shifts. Algae-dominated communities may outcompete coral-dominated communities due to their higher productivity and carbon retention to support fast biomass accumulation while compromising the formation of important reef framework structures. Higher temperatures likely amplify these functional differences, indicating a high vulnerability of ecosystem functions of coral-dominated communities to temperatures even below coral bleaching thresholds. Our results suggest that ocean warming may not only cause but also amplify coral-algal phase shifts in coral reefs.
... Additionally, there is limited information in the literature on mucus release as a consequence of ocean acidification and global warming (Bythell and Wild, 2011); however, during coral bleaching, caused by rising temperatures, an increase in mucus production has been detected (Niggl et al., 2009;Fransolet et al., 2012), possibly resulting in a mucus composition changes (Wooldridge, 2009). ...
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Mucus secretion provides an interface with unique and multifunctional properties between the epithelial cells of many aquatic organisms and their surrounding environment. Indeed, mucus is involved in various essential biological processes including feeding, reproduction, osmoregulation, competition for space, defense against pathogens, xenobiotics, and a multitude of environmental stressors. The ability to produce a functional mucus layer is an important evolutionary step, arising first in Cnidaria that allowed for the development of the mucus-lined digestive cavity seen in higher metazoans. Mucus secretion by cnidarians has been moderately investigated in both corals and jellyfish, which among cnidarians are the ones that have shown the highest secretion rates to date. However, although in corals the production of mucus has received more attention, especially in view of the important ecological role played in coral reefs, in medusozoans the topic is little considered. Although the mucus secreted by corals has innumerable and important immunological, nutritional, and protective responsibilities, it should be remembered that jellyfish too represent a fundamental component of marine trophic web, playing numerous and important roles that are still unclear today. What is certain is that jellyfish are characterized (especially in the era of climate change) by large fluctuations in population density, the ecological implications of which are poorly understood. However, in both cases (Medusozoans and Anthozoans) to date some aspects relating to mucous secretions seem completely obscure, such as the microbiome and its variations as a function of environmental conditions or ontogenetic development, its implications in the field of immunological ecology, the consequent energy costs and finally the role played by the mucus in evolutionary terms. This review summarizes the properties, functions, ecological implications and evolutionary importance of mucus, in cnidarians, mainly focusing its roles in corals and jellyfish. Understanding these aspects relating to the ecological and evolutionary importance played by mucus is of fundamental importance for the ecosystems functioning.
... (b) Examples of compounds belonging to each discipline showing the direct detection of components of the because of the scarcity of specific nutrients necessary for growth (Shick et al. 2011). In turn, these limitations may shape ecological interactions and affect cycling of nutrients within the organism and the ecosystem (Niggl et al. 2009). The bioelemental composition of a species (its elementome) is reflective of environmental change (e.g. ...
Coral reef ecosystems are facing unprecedented anthropogenic pressures, and a highly uncertain future under continued climate change, requiring diverse management options to urgently retain healthy functioning and ecosystem service provisions. Over a decade of innovative research in reef genomics has positioned molecular techniques within reach of rapidly developing reactive reef management approaches and tools. In contrast, analytical techniques that focus on metabolites and their building blocks (elements)—that have proven to be highly informative as tools aiding conservation and restoration efforts of marine and terrestrial ecosystems—remain largely unapplied in the context of coral reefs. This chapter explores the current state of coral reef research using metabolite-based disciplines, covering classical metabolomics, lipidomics and volatilomics (and elemental-based elementomics), and discusses their potential for reef conservation. We suggest that these metabolomic-based approaches can be implemented in coral reef conservation by building on the vast lessons learnt from reef genomics and outline a roadmap of the key steps required to move this field forward: (1) maximise capability among the research community, (2) ensure metabolomic-based disciplines themselves are developed collectively so as to enable greater applicability, and (3) develop these disciplines in parallel to the tools (hardware) needed for management decision-making.KeywordsClimate changeConservationCoral reefElementomicsLipidomicsMetabolomicsStable isotope analysesVolatilomics
... We observed neither a change in the direction nor magnitude of DOC fluxes from coral-dominated communities after nutrient enrichment. This aligns with the common assumption that the release of DOC is closely coupled to productivity (Haas et al., 2011) (although, in corals, DOC release can also be stimulated by stress or as a protective mechanism (Niggl et al., 2009)). Moreover, and unlike previously suggested , we did not observe any change in calcification of coral-dominated communities with moderate nutrient enrichment, neither during light nor dark incubations. ...
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Ecosystem services provided by coral reefs may be susceptible to the combined effects of benthic species shifts and anthropogenic nutrient pollution, but related field studies are scarce. We thus investigated in situ how dissolved inorganic nutrient enrichment, maintained for two months, affected community-wide biogeochemical functions of intact coral-and degraded algae-dominated reef patches in the central Red Sea. Results from benthic chamber incubations revealed 87% increased gross productivity and a shift from net calcification to dissolution in algae-dominated communities after nutrient enrichment, but the same processes were unaffected by nutrients in neighboring coral communities. Both community types changed from net dissolved organic nitrogen sinks to sources, but the increase in net release was 56% higher in algae-dominated communities. Nutrient pollution may, thus, amplify the effects of community shifts on key ecosystem services of coral reefs, possibly leading to a loss of structurally complex habitats with carbonate dissolution and altered nutrient recycling.
Although coral bleaching caused by high temperatures has attracted great concern, the response of the coral microbiome to bleaching has not been thoroughly explored. In this study, bacterial communities from 26 genera of semi-bleached coral in the South China Sea were studied using high-throughput sequencing during El Niño. Principal coordinates analysis (PCoA) indicated that the effect of early bleaching exceeded the effect of coral species on the bacterial communities. Bleaching caused significant changes in coral bacterial communities. Burkholderiales, Caulobacterales, Pseudomonadales, Cytophagales, Oceanospirillales, and Rhodobacterales, were significantly enriched in bleaching coral, whereas Rhizobiales, Cyanobacteria, Microtrichales, Thermoanaerobaculales, Lachnospirales, Rickettsiales, and Lactobacillales, decreased in abundance. Core bacterial OTUs (operational taxonomic units) showed that high temperatures facilitated potentially pathogenic bacteria, such as Alcaligenes, Escherichia, Acinetobacter, Staphylococcus, and Enterobacteriaceae to occupy core positions. Further bleaching resulted in a significant reduction of potential core probiotics in corals. This could increase the risk of corals contracting diseases and reduce their environmental adaptability. Network analysis indicated that the bacterial interactions in bleaching coral were more complex than unbleached coral. Bacteroidales, Burkholderiales, Caulobacterales, Lactobacillales and Rhizobiales were the main taxa that interacted with other bacteria in bleaching and unbleached corals. The presence of these dominant taxa resulted in an increase in chemoheterotrophy, hydrocarbon degradation, nitrogen respiration, and denitrification, which led to great changes in the coral microenvironment. This study comprehensively revealed the response mechanism of coral bacteria during the bleaching process.
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Tropical coral reefs are hotspots of biodiversity, provide important ecosystem services and belong to the most productive ecosystems on earth, although they flourish in oligotrophic, i.e., nutrient-poor waters where nitrogen (N) is scarce. As such, efficient uptake, recycling and removal mechanisms of N by coral reef organisms and substrates, including the key reef ecosystem engineers, the hard corals, are of paramount importance. However, a holistic understanding of microbially performed N cycling is still missing. Previous studies have demonstrated that microbes capable of fixing atmospheric dinitrogen (N2; diazotrophs) provide bioavailable N to the coral reef organisms. Hypothesised counteracting N-removing mechanisms like denitrification, hence, may help to maintain low N conditions, and ultimately coral (reef) functioning. Hence, N availability in coral reef environments is partly a consequence of the interplay between N2 fixation and denitrification, but knowledge particularly on denitrification is missing. As coral reefs and their functioning are adapted to oligotrophic environments, environmental alterations such as eutrophication could potentially evoke ecosystem responses, and subsequently, directly affect biogeochemical pathways. The present thesis aims to extend current knowledge on biogeochemical cycling of N in coral reefs by targeting the following research goals: i) developing a new method to simultaneously determine N2 fixation and denitrification and quantifying N fluxes in and ex situ; ii) assessing baseline rates of N2 fixation and denitrification for major functional groups and assessing their relative importance in intact coral- and degraded algae-dominated reef communities; and iii) investigating the effects of short- and long-term eutrophication on both aforementioned N cycling pathways. Hypothetically, similar to N2 fixation, denitrification is an active microbially performed N cycling pathway in coral reef organisms and substrates, with eutrophication evoking suppressing and stimulating responses, respectively, of N2 fixation and denitrification activity. The experimental work consisted of a combination of physiological and molecular tools and was carried out in situ and ex situ at the central Red Sea. Methods established during the present dissertation allow the simultaneous quantification of N2 fixation and denitrification by combining commonly applied acetylene-based incubation methods. Further, community-wide N fluxes were also quantified in situ using benthic incubation chambers. Findings of the present thesis reveal that denitrification, like N2 fixation, is an active pathway in all investigated coral reef substrates and organisms. On an ecosystem level, important N2 fixers such as turf algae and coral rubble exhibit ~100-fold higher N2 fixation rates compared to corals, but these substrates are less involved in processing nitrogenous compounds via denitrification. On the other hand, soft corals show 2- to 4-fold higher denitrification rates than turf algae or coral rubble and can thus be characterised as key denitrifiers in reef environments. Extrapolated to coral- and algae-dominated reef areas, turf algae and coral rubble contribute to > 90 % of fixed N in both reef areas, whereas > 50 % of total denitrification was performed by corals in degraded reef areas. In situ long-term (8 weeks) eutrophication experiment stimulated both N2 fixation and denitrification in turf algae, a hard coral and reef sands. Further, a substrate-specific and nutrient concentration-dependant threshold that modulates N2 fixation and denitrification in coral rubble was observed, as rapid responses in N cycling activities were observed. In conclusion, using the newly established methods during the thesis, denitrification was identified as an actively performed pathway in coral reef environments. Interestingly and against hypothesis, the effects of eutrophication on N cycling pathways are divergent, with both suppressing and stimulating effects on N2 fixation and denitrification. Altogether, higher N availability in algae-dominated reefs through high amounts of N2 fixation may facilitate higher growth rates of reef algae, ultimately resulting in a positive feedback loop (on the budget of bioavailable N), particularly under moderately and realistic nutrient-enriched scenarios. In contrast, coral rubble may inhibit a key role under very eutrophic conditions, as an N-dependant threshold was identified that stimulates denitrification and suppresses N2 fixation. As such, coral rubble might alleviate excess N from coral reefs via processing N via denitrification. In how far divergent responses of N2 fixation and denitrification to eutrophication might be further suppressed, counteracted or stimulated due to further anthropogenic stressors such as ocean warming remains to be targeted in future studies. Based on the findings here, future management efforts should ultimately focus on the prevention of local N eutrophication.
Coral heads of the genusPlatigyra exposed to low concentrations of crude oil, copper sulfate, potassium phosphate, or dextrose were killed in periods of 5 to 10 days in aquarium studies. The chemicals stimulated the production of large quantities of mucus by the corals. In aquaria treated with antibiotics to prevent microbial growth,Platigyra survived the presence of these chemicals in the water, indicating a role of the microflora in the death of the corals. Evidence was obtained implicating predatory bacteria,Desulfovibrio andBeggiatoa, in the destruction of the stressed coral colonies.
An equation is derived which rigorously defines the photosynthesis : respiration ratio (P:R) for any alga : invertebrate symbiotic association and permits the computation of the fractional contribution of translocated algal carbon to the daily respiratory carbon requirement of the host animal. The equation is applied to two species of symbiotic reef corals, using 0, flux data from 24-h continuous measurements in situ. Given certain assumptions, the algae in the shallow-water Hawaiian reef corals Pocillopora danzicornis and Fungia scutaria can supply of the order of 63 and 69% of the daily respiratory carbon demand of their respective animal hosts.