ArticlePDF Available

Bleaching susceptibility of aquarium corals collected across northern Australia

  • Aquatic Science and Assessment

Abstract and Figures

There are a wide range of Scleractinian corals that are collected for the global reef aquarium market, often from non-reefal environments. The sustainability of coral harvesting is potentially threatened by increasing anthropogenic disturbances and climate change, though it is unknown to what extent many commonly harvested corals are susceptible to environmental change, or actually bleach during marine heatwaves. In this study, we experimentally tested the temperature sensitivity and bleaching susceptibility of six coral species (Homophyllia australis, Micromussa lordhowensis, Catalaphyllia jardinei, Trachyphyllia geoffroyi, Duncanopsammia axifuga, and Euphyllia glabrescens), which are important components of the aquarium coral fisheries across northern Australia, in Western Australia, the Northern Territory, and/or Queensland. Interspecific differences were evident in the temperature sensitivity and bleaching susceptibility among the study species. Homophyllia australis, and M. lordhowensis were found to be particularly susceptible to elevated temperatures, whereby all corals subjected to elevated temperatures died within the course of the experimental treatment (75 d). Catalaphyllia jardinei and E. glabrescens also exhibited significant increases in mortality when exposed to elevated temperatures, though some of the corals did survive, and C. jardinei mostly died only after exposure to elevated temperatures. The other species (T. geoffroyi and D. axifuga) exhibited marked bleaching when exposed to elevated temperatures, but mortality of these corals was similar to that of conspecifics held at ambient temperatures. This study highlights the potential for environmental change to impact the sustainability and viability of Australian coral harvest fisheries. More importantly, this study highlights the need for specific and targeted in situ monitoring for important stocks of coral fishery target species, to assess their vulnerability to fishery and fishery-independent effects.
This content is subject to copyright. Terms and conditions apply.
Bleaching susceptibility of aquarium corals collected
across northern Australia
Morgan S. Pratchett
Ciemon F. Caballes
Stephen J. Newman
Shaun K. Wilson
Vanessa Messmer
Deborah J. Pratchett
Received: 1 December 2019 / Accepted: 15 April 2020 / Published online: 30 April 2020
ÓThe Author(s) 2020
Abstract There are a wide range of Scleractinian corals
that are collected for the global reef aquarium market, often
from non-reefal environments. The sustainability of coral
harvesting is potentially threatened by increasing anthro-
pogenic disturbances and climate change, though it is
unknown to what extent many commonly harvested corals
are susceptible to environmental change, or actually bleach
during marine heatwaves. In this study, we experimentally
tested the temperature sensitivity and bleaching suscepti-
bility of six coral species (Homophyllia australis,Micro-
mussa lordhowensis,Catalaphyllia jardinei,Trachyphyllia
geoffroyi,Duncanopsammia axifuga, and Euphyllia glab-
rescens), which are important components of the aquarium
coral fisheries across northern Australia, in Western Aus-
tralia, the Northern Territory, and/or Queensland. Inter-
specific differences were evident in the temperature
sensitivity and bleaching susceptibility among the study
species. Homophyllia australis, and M. lordhowensis were
found to be particularly susceptible to elevated
temperatures, whereby all corals subjected to elevated
temperatures died within the course of the experimental
treatment (75 d). Catalaphyllia jardinei and E. glabrescens
also exhibited significant increases in mortality when
exposed to elevated temperatures, though some of the
corals did survive, and C. jardinei mostly died only after
exposure to elevated temperatures. The other species (T.
geoffroyi and D. axifuga) exhibited marked bleaching when
exposed to elevated temperatures, but mortality of these
corals was similar to that of conspecifics held at ambient
temperatures. This study highlights the potential for envi-
ronmental change to impact the sustainability and viability
of Australian coral harvest fisheries. More importantly, this
study highlights the need for specific and targeted in situ
monitoring for important stocks of coral fishery target
species, to assess their vulnerability to fishery and fishery-
independent effects.
Keywords Controlled experiment Scleractinia
Temperature Light intensity Survivorship
Mass coral bleaching is an increasingly familiar and
recurring phenomenon, whereby many different species of
zooxanthellate corals lose their endosymbionts and asso-
ciated photosynthetic pigments (Glynn 1984), mainly in
response to environmental stress, including freshwater
inundation, aerial exposure, sedimentation and anomalous
temperatures (Wiedenmann et al. 2013). The severity,
extent and frequency of mass coral bleaching has increased
since the 1980s (Hughes et al. 2018a) in line with ocean
warming and increasing incidence of marine heatwaves
(Heron et al. 2016; Hobday et al. 2018; Skirving et al.
Topic Editor Andrew Hoey
&Morgan S. Pratchett
ARC Centre of Excellence for Coral Reef Studies, James
Cook University, Townsville, QLD 4811, Australia
Western Australian Fisheries and Marine Research
Laboratories, Department of Primary Industries and Regional
Development, Government of Western Australia, Hillarys,
WA 6025, Australia
Marine Science Program, Department of Biodiversity,
Conservation and Attractions, Western Australian
Government, Kensington, WA 6151, Australia
Oceans Institute, University of Western Australia, Crawley,
WA 6009, Australia
Coral Reefs (2020) 39:663–673
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
2019). Marine heatwaves are now the foremost cause of
mass coral bleaching and elevated coral mortality (Hughes
et al. 2018a,b), threatening the population viability of
vulnerable coral species and undermining the ecological
integrity and function of reef ecosystems. Climate-induced
coral bleaching, as well as other causes of coral mortality,
may also directly undermine the sustainability and viability
of harvest fisheries that collect corals from the wild, mainly
for home and public aquaria (Harriott 2003; Rhyne et al.
International ornamental and aquarium coral fisheries
involve the annual trade of hundreds of thousands of small
coral pieces and are worth millions of dollars (Wood et al.
2012). An increasing portion of the coral sold comes from
aquaculture; however the majority is still collected from
the wild, from countries like Indonesia and the Philippines
(Rhyne et al. 2012). In Australia, coral harvesting is a
relatively minor cause of coral loss, and the annual biomass
of coral removed is negligible compared to reef-wide levels
of coral biomass and productivity (Harriott 2003). For the
Queensland Coral Fishery (QCF) the annual Total Allow-
able Commercial Catch (TACC) is 200 tonnes, with fishing
activity spread across a large area, and prohibited within
no-take marine reserves (QDEEDI 2009). Reported catches
have also been \50% of the TACC throughout the last
decade (DAF 2018). Coral fisheries in other jurisdictions
(Western Australia, Northern Territory, and the Coral Sea)
have much smaller quotas. Despite the limited overall
harvesting, it is possible that specific species may be over-
exploited where harvesting is concentrated on rare species.
Aquarium corals are mostly selected based on appearance,
especially colour, as well as their amenability to harvest-
ing, transport and maintenance within aquaria. Few juris-
dictions have species-specific quotas, and there is
insufficient knowledge of wild stocks to even propose
relevant harvest limits for most species (Roelofs and Sil-
cock 2008). Aside from fisheries effects, widespread and
accelerating degradation of coral reef ecosystems is placing
increasing pressure on coral fisheries globally, leading to
greater public and political scrutiny regarding the sustain-
ability of coral harvesting (Albert et al. 2015). The prin-
cipal concern relates to the potential risk of localized
depletion for vulnerable and slow-growing coral species
(Harriott 2003; Garrabou et al. 2017). This concern is
further magnified where harvested corals are simultane-
ously being impacted by fisheries-independent threats,
including rapid and accelerating environmental change
(Montero-Serra et al. 2019). Importantly, marine heat-
waves have caused severe and widespread coral bleaching
across Australia in recent years (Hughes et al. 2017), but it
is largely unknown how these events impacted many of the
corals (other than Acropora spp.) harvested by aquarium
coral fisheries.
All zooxanthellate organisms are susceptible to tem-
perature-induced bleaching at some level (Buddemeier and
Fautin 1993), and very severe marine heatwaves can cause
comprehensive bleaching and mortality across a wide
range of different coral species (e.g., Vargas-Angel et al.
2019). There are however, apparent taxonomic differences
in the susceptibility and responses of corals to increasing
temperature (Loya et al. 2001; Grottoli et al. 2014; Hoey
et al. 2016; Claar and Baum 2019). Among common,
widespread and well-studied coral taxa, the rank order of
bleaching susceptibility (based on the proportion of colo-
nies that bleach or die) appears to be fairly conserved
among geographic locations (e.g., McClanahan et al.
2004), whereby Acropora spp. are often the first to bleach
and experience the highest mortality rates (Baird and
Marshall 2002; Pratchett et al. 2013; Burt et al. 2019; but
see Guest et al. 2012; Chou et al. 2016). Conversely, other
corals, such as Turbinaria spp. are rarely observed to
bleach (e.g., Marshall and Baird 2000) and appear partic-
ularly capable of withstanding thermal stress. There are
many coral taxa for which we know very little about
temperature sensitivity and bleaching susceptibility, mostly
because they do not occur on shallow carbonate reefs,
where in situ studies of coral bleaching are predominantly
conducted (e.g., Hughes et al. 2017; Gilmour et al. 2019;
Raymundo et al. 2019; but see Camp et al. 2018). This
includes many of the coral taxa that are collected for the
aquarium fishery from turbid intertidal habitats.
The purpose of this study was to assess the temperature
sensitivity and bleaching susceptibility of six commonly
harvested aquarium corals (Homophyllia australis,Micro-
mussa lordhowensis,Catalaphyllia jardinei,Trachyphyllia
geoffroyi,Duncanopsammia axifuga, and Euphyllia glab-
rescens), by exposing each of these coral species to ele-
vated temperatures in aquaria. While such experimental
studies are highly constrained in their capacity to assess
how corals respond to elevated temperatures in the wild
(Camp et al. 2018), there is a paucity of data regarding the
bleaching susceptibility of these study species and experi-
mental studies provide the most tractable way to assess
relative bleaching susceptibility of poorly studied species.
Experimental set-up
This study was conducted in the Marine Aquarium
Research Facility (MARFU) at James Cook University, in
Townsville, Australia. Licensed coral collectors in
Queensland (both CQ and NQ), WA and NT provided a
total of 257 distinct corals (mostly whole colonies or
individual polyps, but sometimes fragments) across 6
664 Coral Reefs (2020) 39:663–673
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
different study species (H. australis,M. lordhowensis,C.
jardinei,T. geoffroyi,D. axifuga, and E. glabrescens) that
were transported to Townsville within 1–2 weeks of col-
lection. Where possible, samples of each coral species were
obtained from Western Australia (WA), Northern Territory
(NT), north Queensland (NQ) and central Queensland (CQ)
(Table 1). All corals were mounted on ceramic discs,
which were coded to distinguish individual corals and their
provenance. Corals (1–2 individuals per species per loca-
tion) were randomly assigned to each one of 12 different
tanks across four different treatments (Fig. 1).
To test the bleaching responses and temperature sensi-
tivity of the different corals, corals within the ‘‘heated
treatments’ were subject to gradual warming (1.0 °C
change per week) until the temperature reached a maxi-
mum of 32 °C. The reason for using prolonged heating to
relatively high maximum temperatures was intended to
explicitly assess interspecific and regional variation in
bleaching susceptibility, based on the time until individual
corals exhibited bleaching. Temperatures in control tanks
started at 25.6 °C, and varied between 25.1 and 27.5 °C
through the course of the experiment. Given most of the
study species come from turbid inshore or deeper inter-
reefal habitats, it was possible that bleaching susceptibility
would be moderated by the light environment. To test this,
we further divided corals into high and low light treat-
ments, whereby the maximum light intensity (measured
using a Li-Cor portable light meter during peak irradiance)
was 208.0 (±10.6 SE) and 48.7 (±2.8 SE) lmol m
, respectively. These different light intensities are
equivalent to those used to assess the role of light
([180 lmol m
) in previous experimental bleaching
studies (e.g., Wiedenmann et al. 2013), and are approxi-
mately equivalent to light regimes recorded in open reef
environments versus shaded environments (e.g., within
caves) at a depth of 5 m (Anthony and Hoegh-Guldberg
All colonies were acclimated to experimental conditions
(ambient temperature and low light) for a minimum of
1-week before being subject to high light and/or experi-
mental warming. The day that warming was initiated (April
9th 2018) was set as Day 1, and corals were subject to
experimental conditions until Day 75, at which time
experimental tanks with high temperatures were reduced to
ambient temperatures over 72 h. We then continued to
monitor all surviving colonies until Day 150. Corals were
inspected every 1–2 d to record survival, and scored for
colour, following Siebeck et al. (2006) every 1–2 weeks.
Survival of individual coral colonies was recorded as the
sum of the proportion of time a coral survived during the
heating experiment plus the proportion of time the coral
survived post treatment; i.e. corals that survived to day 75
(end of heating experiment) were assigned a survivorship
of 1.0, and corals that survived to day 150 (end of study
period) were assigned survivorship of 2.0. Changes in
colour were based on changes in colour saturation (mea-
sured on a 6-point scale), between initial records taken on
Day 1 versus Day 75 (or the last record of colour hue taken
prior to mortality). Bleaching was defined as a change in
colour saturation of 2 units or more, following Siebeck
et al. (2006).
Data analyses
We modelled colour change and survival in corals as a
function of ‘Temperature’ and ‘Light’ using linear mixed-
effects models (Bates et al. 2015). ‘Species’, ‘Tempera-
ture’, and ‘Light’ were included as fixed effects. We also
included the individual ‘Tank’ where the corals were
placed as a random effect to account for the non-inde-
pendence of replicates tested within the same aquarium.
‘Region’ was not included as a factor since some species
were only sourced from one locality (see Table 1). Alter-
native models were compared using Akaike’s information
criterion corrected for small sample sizes (AICc) following
Burnham and Anderson (2002). Models were fitted using
the ‘lmer’ function (library lme4) in R 3.0.1 (R Core Team
2019). Post hoc comparisons were conducted for survival
data using the Tukey method in the R package emmeans
(Lenth et al. 2018).
To better resolve differences in survival among corals,
we obtained nonparametric estimates of the shape of the
survivorship curves for each coral species under the two
temperature treatments using Kaplan–Meier product-limit
Table 1 Identity and provenance of corals used in the controlled
bleaching experiment to test for interspecific differences in suscep-
tibility to elevated temperature and light
Species NT NQ CQ WA Total
Family Lobophyllidae
Homophyllia australis 17 17
Micromussa lordhowensis 18 18
Family Merulinidae
Catalaphyllia jardinei 18 20 38
Trachyphyllia geoffroyi 18 23 15 56
Family Dendrophylliidae
Duncanopsammia axifuga 20 18 19 21 78
Family Euphyllidae
Euphyllia glabrescens 18 16 16 50
Total 20 72 113 52 257
Source region: NT Northern Territory (Darwin), NQ North Queens-
land (Cairns), CQ Central Queensland (Mackay), WA Western Aus-
tralia (Karratha). Corals were equally distributed among the four
Coral Reefs (2020) 39:663–673 665
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
Ambient temp.
Low light
Ambient temp.
High light
Low light
High light
H. australisM. lordhowensisC. jardineiT. geoffroyiD. axfugaE. glabrescens j
666 Coral Reefs (2020) 39:663–673
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
analysis. The Kaplan–Meier model is based on estimating
conditional probabilities at each time point when an event
occurs, and taking the product limit of those probabilities
to estimate the survival rate at each point in time (Kaplan
and Meier 1958). Survival probabilities were calculated
using the ‘survfit’ function in the R package survival
(Therneau 2015) and visualised by plotting survival curves
using the ‘ggsurvplot’ function in the R package survminer
(Kassambara et al. 2017). To test whether survival trends
were significantly different for each treatment, survival
probabilities were compared using the Log-rank test, which
takes into account both individuals that died during the
course of the experiment and individuals that were still
alive at the end of the study, i.e. right-censored data
(Walker and Shostak 2010). All plots and analyses were
implemented in R 3.0.1 (R Core Team 2019).
To assess interspecific and regional variation in the
tolerance of corals to temperature and light treatments,
standardised mean differences (SMDs), using Hedges’
G(Hedges 1981) as an effect size metric, were calculated
using the ‘metacont’ function in the R package meta
(Schwarzer 2007). Calculated effect sizes and 95% confi-
dence intervals were used to generate forest plots in R 3.0.1
(R Core Team 2019).
Bleaching susceptibility
A total of 257 small (\60 mm diameter) corals were used
in the experiment (Table 1). Of these, 128 (49.8%) corals
exhibited declines in colour saturation through the course
of the experiment, with bleaching (where declines in colour
saturation were [2) recorded for 74 corals (28.8%). All
six species exhibited bleaching (Fig. 2). The incidence of
bleaching was consistently higher for corals subject to
experimental warming (35.6%), though 16.67% of the
colonies maintained at ambient temperatures also bleached
(Fig. 2). The overall incidence of bleaching (across all
treatments) was greatest for M. lordhowensis (38.9%,
n= 18) and E. glabrescens (38.0%, n= 50). Lower inci-
dence of bleaching was recorded for C. jardinei (26.3%,
n= 38) and T. geoffroyi (23.2%, n= 56), and particularly
for H. australis (17.6%, n= 17) and D. axifuga (11.5%,
n= 78). For D. axifuga, bleaching incidence ranged from
10 to 17% with no obvious regional differences. For E.
glabrescens, however, it was notable that only colonies
collected from the GBR (NQ and CQ) exhibited bleaching
(even when exposed to high light at ambient temperatures),
whereas none of the colonies from WA exhibited major
colour loss even when exposed to elevated temperature.
The best models to explain variation in the extent of
colour loss recorded during this study included ‘Species’,
‘Temperature’, ‘Light’, and the interaction between
‘Temperature’ and ‘Light’ (Table 2). For M. lordhowensis,
C. jardinei,T. geoffroyi and D. axifuga, bleaching (declines
in colour saturation [2) was more prevalent and more
pronounced for corals subject to warming, but the extent of
colour loss was also exacerbated by exposure to high light
(Fig. 2). Based on standardised mean differences, elevated
temperature resulted in significant colour change for C.
jardinei,T. geoffroyi, and D. axifuga, while high light
intensity accounted for significant colour loss in M. lord-
howensis and D. axifuga (Fig. 3). For E. glabrescens, the
median level of colour loss was greatest in the high tem-
perature and high light treatment, but bleaching was
recorded across all treatments (Fig. 2). For H. australis, the
incidence of bleaching was low across all treatments
(Fig. 2).
Eighty-five (out of 257; 33.1%) corals survived to the end
of the experiment (150 d). Survivorship was lower (21.3%)
among corals subject to warming, than for corals main-
tained at ambient temperatures (57.8%). However, there
was also marked interspecific variation in the survival of
corals between the two temperature treatments. The best
model (based on wAICc) for explaining variation in sur-
vivorship included the interaction between ‘Species’ and
‘Temperature’, but did not include light levels (Table 2).
Post hoc pairwise comparisons showed that there were
significant differences in survival between corals subject to
warming versus ambient temperatures for H. australis
(p\0.001), M. lordhowensis (p\0.001), C. jardinei
(p= 0.028), and E. glabrescens (p\0.001); but not for T.
geoffroyi (p= 0.791) and D. axifuga (p= 0.270).
Survivorship of the different coral species varied both in
extent and timing. For H. australis and M. lordhowensis,
survival declined sharply from day 1 to day 75, during the
treatment period for corals subject to warming (Fig. 4).
Importantly, many colonies of H. australis died without
exhibiting prior bleaching. For C. jardinei and E. glab-
rescens, there were also significant differences in survival
with respect to temperature treatments, though this differ-
ence was most pronounced after the recovery period, on
Day 150. For C. jardinei, differences in survival between
temperature treatments were limited (92% vs. 81%) during
bFig. 1 Select images of experimental colonies to indicate interspeci-
fic differences in responses of the six coral species (H. australis,M.
lordhowensis,C. jardinei,T. geoffroyi,D. axifuga, and E.
glabrescens) with exposure to increasing temperature and high levels
of light intensity
Coral Reefs (2020) 39:663–673 667
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
the treatment period, from day 1 to day 75, but overall
survivorship (at day 150) was much lower for corals
subjected to warming (19%) compared to colonies main-
tained at ambient temperatures (75%) (Fig. 4c). There was
Low High
(a) Homophyllia australis
Low High
(b) Micromussa lordhowensis
Low High
Colour Change
(c) Catalaphyllia jardinei
Low High
(d) Trachyphyllia geoffroyi
Low High
Light Intensity
(e) Duncanopsammia axifuga
Low High
(f) Euphyllia glabrescens
Temperature: Ambient Hot
Fig. 2 Boxplots showing species-specific colour change response to
temperature and light intensity treatments. Plots show median (bold
line), 25th and 75th percentile range (box), 5th and 95th percentile
range (error bars), and jitter points (large coloured circles) pooled
across temperature treatments for each light treatment
668 Coral Reefs (2020) 39:663–673
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
no difference in survival of T. geoffroyi or D. axifuga with
respect to temperature treatments (Fig. 4). For D. axifuga,
\50% of corals survived 50 d, and there was ongoing
mortality throughout the subsequent treatment and recov-
ery period (Fig. 4e). Survival of T. geoffroyi was much
higher than for D. axifuga, but there were sustained levels
of mortality throughout the experiment both for corals
exposed to elevated temperatures and those maintained at
ambient temperatures (Fig. 4).
Based on standardised mean differences, elevated tem-
perature had a substantial negative effect on the survival of
H. australis (as well as for M. lordhowensis, which was
excluded from analyses due to zero variance in the ‘Am-
bient’ treatment, i.e. 100% survival) and E. glabrescens
(Fig. 3). Warming also had a moderate effect on the sur-
vival of C. jardinei, but we did not observe any adverse
effect on T. geoffroyi and D. axifuga. For those species that
did exhibit significant differences in survival between
temperature treatments, interspecific differences in tem-
perature sensitivity are also reflected in the time to median
(50%) survival, which was lowest for H. australis (51 d),
but also \75 d for M. lordhowensis (58 d) and E. glab-
rescens (60 d), and longest for C. jardinei (118 d).
This study explored the temperature sensitivity and
bleaching susceptibility of six different coral species (H.
australis,M. lordhowensis,C. jardinei,T. geoffroyi,D.
axifuga, and E. glabrescens), which are important target
species for aquarium fisheries in QLD, WA and/or NT
(DEEDI 2012; DPIR 2019; Newman et al. 2019). All six
corals species exhibited bleaching to a greater or lesser
Light Intensity Effect Size
on Colour Change
Temperature Effect Size
on Colour Change
Temperature Effect Size
on Survival
−3 −2 −1 0 1 −3 −2 −1 0 1 −25 −20 −15 −10 −5 0
H. australis
M. lordhowensis
C. jardinei
T. geoffroyi
D. axifuga
E. glabrescens
Fig. 3 Inter-specific differences in the effect of light intensity and
temperature on colour change and the effect of high temperature on
survival, based on Hedge’s G(i.e. effect size). Red dashed line
indicates zero effect, while points to the left of this line suggest a
negative treatment effect on colour change or survival
Table 2 Linear mixed-effects
model (LMM) results for
(a) survival and (b) colour
change predicted as a function
of ‘Species’, ‘Temperature’,
‘Lighting’, and their interaction
Model df LL AICc wAICc Adj R
(a) Colour change
Species ?temperature ?light ?(1 | Tank) 10 -421.3 863.5 0.347 0.229
Species ?temperature 9light ?(1 | Tank) 11 -420.7 864.5 0.207 0.229
(1|| Tank) 3 -432.5 871.1 0.008 0.131
Species 9temperature 9light ?(1 | Tank) 26 -410.0 878.2 0.000 0.253
(b) Survival
Species 9temperature ?(1 | Tank) 14 -177.3 384.3 0.922 0.535
Species 9temperature 9light ?(1 | Tank) 26 -179.3 416.8 0.000 0.555
(1 | Tank) 3 -232.4 471.0 0.000 0.080
All models include the tank as the random effect. Shown above are the degrees of freedom (df), maximum
log-likelihood (LL), Akaike’s information criterion corrected for small sample sizes (AICc), AICc weight
(wAICc), and the adjusted R
(adj R
). Only models with DAICc\2 are shown, in addition to the saturated
and null models, and are ordered by increasing AICc
Coral Reefs (2020) 39:663–673 669
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
p < 0.001
0 25 50 75 100 125 150
p < 0.001
0 25 50 75 100 125 150
p < 0.001
0 25 50 75 100 125 150
p = 0.003
0 25 50 75 100 125 150
Survival Probability
p = 0.560
0 25 50 75 100 125 150
p = 0.360
0 25 50 75 100 125 150
Time (da
Temperature: Ambient Hot
(a) Homophyllia australis (b) Micromussa lordhowensis
(c) Catalaphyllia jardinei (d) Trachyphyllia geoffroyi
(e) Duncanopsammia axifuga (f) Euphyllia glabrescens
670 Coral Reefs (2020) 39:663–673
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
extent. Most notably, M. lordhowensis, C. jardinei, D.
axifuga and T. geoffroyi exhibited significant colour loss
(or bleaching) when exposed to elevated temperatures, and
bleaching was exacerbated by high light intensity for M.
lordhowensis and. D. axifuga. Even more concerning
however, were the high levels of coral mortality ([80%)
recorded for H. australis,M. lordhowensis,E. glabrescens
and C. jardinei when these corals were subjected to ele-
vated temperatures. Maximum temperatures to which cor-
als were exposed in this experiment (32 °C) were high,
though corals living in the shallow subtidal and intertidal
zones in northern Australia may be exposed to tempera-
tures C32 °C during severe heatwaves (Moore et al. 2012)
or in areas where water pools for extended periods at low
tide (Dandan et al. 2015).
While bleaching is commonly recorded among sclerac-
tinian corals exposed to elevated temperatures and/or high
light intensity, there are marked interspecific differences in
the responses of corals (Loya et al. 2001; Hueerkamp et al.
2001; Dandan et al. 2015; Hughes et al. 2018b). In this
study, H. australis was extremely sensitive to elevated
temperature, whereby all colonies subjected to elevated
temperatures had died within 60 d, even though this spe-
cies rarely exhibited bleaching. Rather than losing colour,
tissues of H. australis would retract in response to warming
(Fig. 1) prior to complete mortality of the corals. Con-
versely, T. geoffroyi exhibited a high incidence of bleach-
ing when exposed to elevated temperatures, but low levels
of mortality (\50%). We observed yet another response
for C. jardinei, for which, tissues would often detach from
the underlying skeleton when subject to elevated temper-
ature (Fig. 1). In many instances, the free-living tissue
persisted ex situ and retained its colour intensity for the
duration of the experiment. However, this is likely to be an
experimental artefact, as free-living tissues of C. jardinei
would likely be vulnerable to smothering or predation once
dislodged in the wild. The only corals that exhibited more
pronounced bleaching with increased light intensity were
M. lordhowensis and D. axifuga, but this did not translate
to differences in survivorship. Temperature and light act
synergistically to influence bleaching susceptibility (Jokiel
and Coles 1990), such that high turbidity in some nearshore
environments may actually moderate bleaching-induced
mortality during marine heatwaves (e.g., Fisher et al. 2019;
Teixeira et al. 2019). However, this study shows that ele-
vated temperatures are the predominant cause of bleaching
and mortality, and the overriding concern for the corals
considered in this study.
Interspecific differences in the environmental sensitivity
and bleaching susceptibility among the six study species
(H. australis,M. lordhowensis,C. jardinei,T. geoffroyi,D.
axifuga, and E. glabrescens) may partially account for
apparent differences in their abundance in different regions
and habitats, or at least reflect the limited area over which
corals were collected. Notably, the two coral species that
were most susceptible to experimental warming (H. aus-
tralis and M. lordhowensis) were provided exclusively
from CQ, having been collected from the southern GBR in
areas where these corals are relatively abundant. Both these
corals are distributed further north on the GBR in much
warmer waters (Veron et al. 2019), and it is possible that
colonies from lower latitudes might exhibit greater resi-
lience to elevated temperatures (sensu Hoegh-Guldberg
1999). Accordingly, E. glabrescens collected from WA
exhibited much greater resilience to changing temperatures
and light regimes, than conspecifics from the GBR. How-
ever, there was limited evidence of geographical variation
in temperature sensitivity and bleaching susceptibility for
D. axifuga (which was sampled from all four locations),
nor for T. geoffroyi (sampled from WA, NQ and CQ).
Although, this experiment did not specifically account for
local temperature regimes from where individual corals
were collected (and then test bleaching susceptibility
against regionally specific bleaching thresholds), we would
have expected that corals provided from lower latitudes
and warmer water in WA and NT would be more resistant
to elevated temperatures than corals from CQ (sensu
Hoegh-Guldberg 1999). Ultimately, it would be best to
explicitly account for the specific environmental conditions
in habitats from where each individual coral was collected,
but this was not possible given that corals were provided by
licenced coral collectors and their individual provenance
was only broadly known.
This study shows that at least some Australian aquarium
coral fishery target species (specifically, H. australis,M.
lordhowensis,E. glabrescens and C. jardinei) are suscep-
tible to elevated temperatures, thereby highlighting the
potential for sustained and ongoing environmental change
to undermine the sustainability and viability of these fish-
eries. More importantly, there is an increasing shift in
aquarium coral collections and exports towards small polyp
coral species (mainly, Acropora spp., Dee et al. 2014;
Barton et al. 2017) which are, in general, even more sus-
ceptible to environmental change (Baird and Marshall
2002; Pratchett et al. 2013; Hughes et al. 2018b; Burt et al.
2019), though vulnerability assessments will need to be
undertaken for the specific species that are targeted and
habitats from which they are taken. Similarly, results for
this preliminary experimental study should not be used to
bFig. 4 Species-specific Kaplan–Meier-estimated survival probabili-
ties under two temperature treatments. pvalues for the log-rank test
comparing survival curves between ‘Ambient’ and ‘Hot’ treatments
are shown. Dashed line indicates termination of experimental
treatments and start of recovery period at 75 d
Coral Reefs (2020) 39:663–673 671
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
infer relative or absolute vulnerability of the coral fishery
target species to ocean warming, marine heatwaves, or
changing environmental conditions. Rather, this study
highlights the need for specific and targeted in situ moni-
toring for important stocks of coral fishery target species, to
assess their vulnerability to fishery and fishery-independent
Acknowledgements This study was funded in part by the Fisheries
Research and Development Corporation (FRDC; Project 2014-029),
with additional support from the WA Government Department of
Biodiversity, Conservation and Attractions and also Pro-Vision Reef.
In-kind support, through the provision of samples, was provided by
many licensed coral collectors in WA, NT and QLD. Experimental
studies were conducted at the JCU Marine Aquarium Research
Facility (MARFU), and we are grateful to all MARFU staff for sig-
nificant logistic support.
Open Access This article is distributed under the terms of the
Creative Commons Attribution 4.0 International License (http://crea, which permits unrestricted use,
distribution, and reproduction in any medium, provided you give
appropriate credit to the original author(s) and the source, provide a
link to the Creative Commons license, and indicate if changes were
Albert JA, Olds AD, Albert S, Cruz-Trinidad A, Schwarz AM (2015)
Reaping the reef: provisioning services from coral reefs in
Solomon Islands. Marine Policy 62:244–251
Anthony KR, Hoegh-Guldberg O (2003) Variation in coral photo-
synthesis, respiration and growth characteristics in contrasting
light microhabitats: an analogue to plants in forest gaps and
understoreys? Functional Ecology 17(2):246–259
Baird AH, Marshall PA (2002) Mortality, growth and reproduction in
scleractinian corals following bleaching on the Great Barrier
Reef. Mar Ecol Prog S 237:133–141
Barton JA, Willis BL, Hutson KS (2017) Coral propagation: a review
of techniques for ornamental trade and reef restoration. Reviews
in Aquaculture 9(3):238–256
Bates D, Ma
¨chler M, Bolker BM, Walker SC (2015) Fitting linear
mixed-effects models using lme4. Journal of Statistical Software
Buddemeier RW, Fautin DG (1993) Coral bleaching as an adaptive
mechanism. Bioscience 43(5):320–326
Burnham KP, Anderson DR (2002) Model selection and multimodel
inference: a practical information-theoretic approach. Springer,
New York
Burt JA, Paparella F, Al-Mansoori N, Al-Mansoori A, Al-Jailani H
(2019) Causes and consequences of the 2017 coral bleaching
event in the southern Persian/Arabian Gulf. Coral Reefs
Camp EF, Schoepf V, Mumby PJ, Hardtke LA, Rodolfo-Metalpa R,
Smith DJ, Suggett DJ (2018) The future of coral reefs subject to
rapid climate change: lessons from natural extreme environ-
ments. Frontiers Mar Sci 5:4
Chou LM, Toh TC, Toh KB, Ng CS, Cabaitan P, Tun K, Goh E, Afiq-
Rosli L, Taira D, Du RC, Loke HX (2016) Differential response
of coral assemblages to thermal stress underscores the complex-
ity in predicting bleaching susceptibility. PloS ONE
Claar DC, Baum JK (2019) Timing matters: survey timing during
extended heat stress can influence perceptions of coral suscep-
tibility to bleaching. Coral Reefs 38(4):559–565
DAF (2018) Queensland fisheries summary—October 2018. State of
Queensland, Department of Agriculture and Fisheries. https://
Accessed 26 Nov 2019
Dandan SS, Falter JL, Lowe RJ, McCulloch MT (2015) Resilience of
coral calcification to extreme temperature variations in the
Kimberley region, northwest Australia. Coral Reefs
Dee LE, Horii SS, Thornhill DJ (2014) Conservation and manage-
ment of ornamental coral reef wildlife: successes, shortcomings,
and future directions. Biol Cons 169:225–237
DEEDI (2012) Annual status report 2011, Queensland Coral Fishery.
State of Queensland, Department of Employment, Economic
Development and Innovation.
data/assets/pdf_file/0010/76978/ASR_QCF2011.pdf. Accessed
26 Nov 2019
DPIR (2019) Northern Territory Aquarium Fishery Re-Assessment
Report—August 2019. Department of Primary Industry and
Resources, Northern Territory Government. 13p. http://www.
pdf. Accessed 26 Nov 2019
Fisher R, Bessell-Browne P, Jones R (2019) Synergistic and
antagonistic impacts of suspended sediments and thermal stress
on corals. Nature Comm 10(1):1–9
Garrabou J, Sala E, Linares C, Ledoux JB, Montero-Serra I, Dominici
JM, Kipson S, Teixido
´N, Cebrian E, Kersting DK, Harmelin JG
(2017) Re-shifting the ecological baseline for the overexploited
Mediterranean red coral. Sci Rep 7:42404
Glynn PW (1984) Widespread coral mortality and the 1982/83 El
Nino warming event. Env Cons 11:133–146
Grottoli AG, Warner ME, Levas SJ, Aschaffenburg MD, Schoepf V,
McGinley M, Baumann J, Matsui Y (2014) The cumulative
impact of annual coral bleaching can turn some coral species
winners into losers. Global Change Biol 20(12):3823–3833
Guest JR, Baird AH, Maynard JA, Muttaqin E, Edwards AJ et al
(2012) Contrasting patterns of coral bleaching susceptibility in
2010 suggest an adaptive response to thermal stress. PLoS ONE
Gilmour JP, Cook KL, Ryan NM, Puotinen ML, Green RH, Shedrawi
G, Hobbs JP, Thomson DP, Babcock RC, Buckee J, Foster T
(2019) The state of Western Australia’s coral reefs. Coral Reefs
Harriott VJ (2003) Can corals be harvested sustainably? AMBIO
Hedges LV (1981) Distribution theory for Glass’s estimator of effect
size and related estimators. J Ed Behav Stat 6:107–128
Heron SF, Maynard JA, Van Hooidonk R, Eakin CM (2016) Warming
trends and bleaching stress of the world’s coral reefs 1985–2012.
Sci Rep 6:38402
Hobday AJ, Oliver EC, Gupta AS, Benthuysen JA, Burrows MT,
Donat MG, Holbrook NJ, Moore PJ, Thomsen MS, Wernberg T,
Smale DA (2018) Categorizing and naming marine heatwaves.
Oceanography 31(2):162–173
Hoegh-Guldberg O (1999) Climate Change, coral bleaching and the
future of the world’s coral reefs. Mar Freshw Res 50:839–866
Hoey AS, Howells E, Johansen JL, Hobbs JPA, Messmer V,
McCowan DM, Wilson SK, Pratchett MS (2016) Recent
advances in understanding the effects of climate change on
coral reefs. Diversity 8(2):12
672 Coral Reefs (2020) 39:663–673
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
Hueerkamp C, Glynn PW, D’Croz L, Mate
´JL, Colley SB (2001)
Bleaching and recovery of five eastern Pacific corals in an El
˜o-related temperature experiment. Bull Mar Sci
Hughes TP, Kerry JT, A
´lvarez-Noriega M, A
´lvarez-Romero JG,
Anderson KD, Baird AH, Babcock RC, Beger M, Bellwood DR,
Berkelmans R, Bridge TC, Butler IR, Byrne M, Cantin NE,
Comeau S, Connolly SR, Cumming GS, Dalton SJ, Diaz-Pulido
G, Eakin CM, Figueira WF, Gilmour JP, Harrison HB, Heron
SF, Hoey AS, Hobbs J-PA, Hoogenboom MO, Kennedy EV,
Kuo C-y, Lough JM, Lowe RJ, Liu G, McCulloch MT, Malcolm
HA, McWilliam MJ, Pandolfi JM, Pears RJ, Pratchett MS,
Schoepf V, Simpson T, Skirving WJ, Sommer B, Torda G,
Wachenfeld DR, Willis BL, Wilson SK (2017) Global warming
and recurrent mass bleaching of corals. Nature
Hughes TP, Anderson KD, Connolly SR, Heron SF, Kerry JT, Lough
JM, Baird AH, Baum JK, Berumen ML, Bridge TC, Claar DC,
Eakin CM, Gilmour JP, Graham NAJ, Harrison H, Hobbs JPA,
Hoey AS, Hoogenboom M, Lowe RJ, McCulloch MT, Pandolfi
JM, Pratchett MS, Schoepf V, Torda G, Wilson SK (2018a)
Spatial and temporal patterns of mass bleaching of corals in the
Anthropocene. Science 359(6371):80–83
Hughes TP, Kerry JT, Baird AH, Connolly SR, Dietzel A, Eakin CM,
Heron SF, Hoey AS, Hoogenboom MO, Liu G, McWilliam MJ,
Pears RJ, Pratchett MS, Skirving WJ, Stella JS, Torda G (2018b)
Global warming transforms coral reef assemblages. Nature
Jokiel PL, Coles SL (1990) Response of Hawaiian and other Indo-
Pacific reef corals to elevated temperature. Coral Reefs
Kaplan EL, Meier P (1958) Nonparametric estimation from incom-
plete observations. J Am Stat Assoc 53:457–481
Kassambara A, Kosinski M, Biecek P (2017) survminer: Drawing
Survival Curves using ‘ggplot2’. R package version 0.3.1
Lenth R, Singmann H, Love J, Buerkner P, Herve M (2018)
Emmeans: estimated marginal means, aka least-squares means.
Version 1(4):2
Loya Y, Sakai K, Yamazato K, Nakano Y, Sambali H, van Woesik R
(2001) Coral bleaching: the winners and the losers. Ecology
letters 4(2):122–131
Marshall PA, Baird AH (2000) Bleaching of corals on the Great
Barrier Reef: differential susceptibilities among taxa. Coral
Reefs 19(2):155–163
McClanahan TR, Baird AH, Marshall PA, Toscano MA (2004)
Comparing bleaching and mortality responses of hard corals
between southern Kenya and the Great Barrier Reef, Australia.
Marine Pollution Bulletin 48(3–4):327–335
Moore JA, Bellchambers LM, Depczynski MR, Evans RD, Evans SN,
Field SN, Friedman KJ, Gilmour JP, Holmes TH, Middlebrook
R, Radford BT (2012) Unprecedented mass bleaching and loss of
coral across 12 of latitude in Western Australia in 2010–11.
PLoS ONE 7(12):e51807
Montero-Serra I, Garrabou J, Doak DF, Ledoux JB, Linares C (2019)
Marine protected areas enhance structural complexity but do not
buffer the consequences of ocean warming for an overexploited
precious coral. Journal of Applied Ecology 56(5):1063–1074
Newman SJ, Bruce C, Kalinowski P (2019) Statewide Marine
Aquarium Fish and Hermit Crab Resources Status Report 2018.
pp. 199-203. In: Gaughan DJ, Santoro K (eds.). Status reports of
the fisheries and aquatic resources of Western Australia
2017/18: State of the Fisheries. Department of Primary
Industries and Regional Development, Western Australia, Perth,
Australia. 240 pp
Pratchett MS, McCowan D, Maynard JA, Heron SF (2013) Changes
in bleaching susceptibility among corals subject to ocean
warming and recurrent bleaching in Moorea, French Polynesia.
PLoS ONE 8(7):e70443
Queensland Government Department of Employment, Economic
Development and Innovation (QDEEDI) (2009) A guide to the
Queensland Marine Aquarium Fish Fishery and the Queensland
Coral Fishery. 55 pp
Raymundo LJ, Burdick D, Hoot WC, Miller RM, Brown V, Reynolds
T, Gault J, Idechong J, Fifer J, Williams A (2019) Successive
bleaching events cause mass coral mortality in Guam, Microne-
sia. Coral Reefs 38(4):677–700
R Core Team (2019) R: a language and environment for statistical
computing. R Foundation for Statistical Computing, Vienna,
Roelofs A, Silcock R (2008) A Vulnerability Assessment of Coral
Taxa Collected in the Queensland Coral Fishery. Department of
Primary Industries and Fisheries, Brisbane. 10 pp
Rhyne AL, Tlusty MF, Kaufman L (2012) Long-term trends of coral
imports into the United States indicate future opportunities for
ecosystem and societal benefits. Conservation Letters
Schwarzer G (2007) Meta: an R Package for Meta-Analysis. R News
Siebeck UE, Marshall NJ, Klu
¨ter A, Hoegh-Guldberg O (2006)
Monitoring coral bleaching using a colour reference card. Coral
Reefs 25(3):453–460
Skirving WJ, Heron SF, Marsh BL, Liu G, De La Cour JL, Geiger EF,
Eakin CM (2019) The relentless march of mass coral bleaching:
a global perspective of changing heat stress. Coral Reefs.
Teixeira CD, Leita
˜o RL, Ribeiro FV, Moraes FC, Neves LM, Bastos
AC, Pereira-Filho GH, Kampel M, Salomon PS, Sa
Falsarella LN (2019) Sustained mass coral bleaching
(2016–2017) in Brazilian turbid-zone reefs: taxonomic, cross-
shelf and habitat-related trends. Coral Reefs 38(4):801–813
Therneau T (2015) A Package for Survival Analysis in S. version
2.38, Accessed
26 Nov 2019
Vargas-Angel B, Huntington B, Brainard RE, Venegas R, Oliver T,
Barkley H, Cohen A (2019) El Nino-associated catastrophic
coral mortality at Jarvis Island, central Equatorial Pacific. Coral
Reefs. 38(4):731–741
Veron JEN, Stafford-Smith MG, Turak E, DeVantier LM (2019).
Corals of the World. Accessed 22 November 2019, Version 001. [v0.01(Beta)]
Walker GA, Shostak J (2010) Common statistical methods for clinical
research with SAS
examples. 3rd edition. Third. Cary, N.C.,
USA: SAS Institute Inc.
Wiedenmann J, D’Angelo C, Smith EG, Hunt AN, Legiret F-E, Postle
AD, Achterberg EP (2013) Nutrient enrichment can increase the
susceptibility of reef corals to bleaching. Nat Clim Chang
Wood E, Malsch K, Miller J (2012) International trade in hard corals:
review of management, sustainability and trends. Proc. 12th Int.
Coral Reef Symp. 1:9–13
Publisher’s Note Springer Nature remains neutral with regard to
jurisdictional claims in published maps and institutional affiliations.
Coral Reefs (2020) 39:663–673 673
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
Terms and Conditions
Springer Nature journal content, brought to you courtesy of Springer Nature Customer Service Center GmbH (“Springer Nature”).
Springer Nature supports a reasonable amount of sharing of research papers by authors, subscribers and authorised users (“Users”), for small-
scale personal, non-commercial use provided that all copyright, trade and service marks and other proprietary notices are maintained. By
accessing, sharing, receiving or otherwise using the Springer Nature journal content you agree to these terms of use (“Terms”). For these
purposes, Springer Nature considers academic use (by researchers and students) to be non-commercial.
These Terms are supplementary and will apply in addition to any applicable website terms and conditions, a relevant site licence or a personal
subscription. These Terms will prevail over any conflict or ambiguity with regards to the relevant terms, a site licence or a personal subscription
(to the extent of the conflict or ambiguity only). For Creative Commons-licensed articles, the terms of the Creative Commons license used will
We collect and use personal data to provide access to the Springer Nature journal content. We may also use these personal data internally within
ResearchGate and Springer Nature and as agreed share it, in an anonymised way, for purposes of tracking, analysis and reporting. We will not
otherwise disclose your personal data outside the ResearchGate or the Springer Nature group of companies unless we have your permission as
detailed in the Privacy Policy.
While Users may use the Springer Nature journal content for small scale, personal non-commercial use, it is important to note that Users may
use such content for the purpose of providing other users with access on a regular or large scale basis or as a means to circumvent access
use such content where to do so would be considered a criminal or statutory offence in any jurisdiction, or gives rise to civil liability, or is
otherwise unlawful;
falsely or misleadingly imply or suggest endorsement, approval , sponsorship, or association unless explicitly agreed to by Springer Nature in
use bots or other automated methods to access the content or redirect messages
override any security feature or exclusionary protocol; or
share the content in order to create substitute for Springer Nature products or services or a systematic database of Springer Nature journal
In line with the restriction against commercial use, Springer Nature does not permit the creation of a product or service that creates revenue,
royalties, rent or income from our content or its inclusion as part of a paid for service or for other commercial gain. Springer Nature journal
content cannot be used for inter-library loans and librarians may not upload Springer Nature journal content on a large scale into their, or any
other, institutional repository.
These terms of use are reviewed regularly and may be amended at any time. Springer Nature is not obligated to publish any information or
content on this website and may remove it or features or functionality at our sole discretion, at any time with or without notice. Springer Nature
may revoke this licence to you at any time and remove access to any copies of the Springer Nature journal content which have been saved.
To the fullest extent permitted by law, Springer Nature makes no warranties, representations or guarantees to Users, either express or implied
with respect to the Springer nature journal content and all parties disclaim and waive any implied warranties or warranties imposed by law,
including merchantability or fitness for any particular purpose.
Please note that these rights do not automatically extend to content, data or other material published by Springer Nature that may be licensed
from third parties.
If you would like to use or distribute our Springer Nature journal content to a wider audience or on a regular basis or in any other manner not
expressly permitted by these Terms, please contact Springer Nature at
... In Queensland, the fisheries sectors most likely to be sensitive to coral loss are the reef line fishery and the aquarium fishery. This sensitivity of this aquarium sector is well recognized, because catches include live coral 28 , as well as a range of fish species that strongly depend on live corals 29,30 and anemones (which also bleach) 31 . The aquarium fishery has a coral stress response plan that is widely endorsed by the fishing industry 32 . ...
... Amphiprion species (anemonefish) were also included in the high vulnerability category (4), because they are sensitive to bleaching of their host species 31 . All coral was considered category 4 28 . Results are presented for catches across the five Mapstone regions where the fishery operates, but we excluded coral pieces from these graphs. ...
Full-text available
Coral reefs have been subject to mass coral bleaching, potentially causing rapid and widespread degradation of ecosystem services that depend on live coral cover, such as fisheries catch. Fisheries species in tropical waters associate with a wide range of habitats, so assessing the dependency of fisheries on coral reefs is important for guiding fishery responses to coral reef degradation. This study aimed to determine how fisheries catches associate with coral reefs in Queensland, Australia. Queensland's largest fisheries did not target fish associated with reefs, but specific sectors, particularly aquarium fisheries and commercial fisheries in the mid to northern region had a high dependence on species that use coral reefs. Regions that had a greater relative area of coral reefs had higher catches of species that depend on live coral, suggesting that coral area could be used to predict the sensitivity of a jurisdiction's fisheries to bleaching. Dynamic analysis of stock trends found that coral trout and red throat emperor, the two largest species by catch for the reef line fishery, were at risk of overfishing if habitat loss caused declines in stock productivity. Management of fisheries that are highly dependent on reefs may need to adapt to declining productivity, but further research to support ongoing reforms in Queensland's fisheries is needed to quantitatively link reef degradation to stock production parameters is needed.
... For example, responses to thermal stress, which are involved in bleaching, have been examined in terms of physiological aspects, such as symbiotic algal density, algal chlorophyll content, and maximum photosynthetic efficiency (Nielsen et al., 2018;Ben-Zvi et al., 2020). Furthermore, mortality after bleaching and the degree of bleaching have been examined (Pratchett et al., 2020). These stress responses occur in genera-and species-specific manner (Abrego et al., 2008;Diaz et al., 2016;Dias et al., 2019), and the susceptibility of corals to thermal stress has been considered as a critical factor affecting the community structure of coral reef ecosystems (Marshall and Baird, 2000;Dias et al., 2018). ...
Full-text available
Mesophotic habitats are potential refugia for corals in the context of climate change. The seawater temperature in a mesophotic habitat is generally lower than in a shallow habitat. However, the susceptibility and threshold temperatures of mesophotic corals are not well understood. We compared 11 mesophotic and shallow species to understand their thermal stress thresholds using physiological parameters. Coral fragments were exposed to two thermal stress treatments, with temperatures set at ~30°C and ~31°C, and a low-temperature treatment set at ~28 °C as the "no stress" condition for 14 days. We found that the threshold temperature of coral species at mesophotic depths is slightly lower or equal to that of corals in shallow depths. The results suggest that species in the mesophotic coral ecosystems can survive low (<4 degree heating weeks) thermal stress. However, mass bleaching and high mortality can be expected when temperatures rise above 4 degree heating weeks.
... The QCF has the largest annual Total Allowable Commercial Catch (TACC) of all Australian coral fisheries at 200 t, which is split between 60 t of 'specialty' or LPS corals and 140 t of 'other' corals; which includes branching taxa such as the Acroporidae 15 . Concerns have previously been raised regarding the potential for the localised depletion of specific coral species in areas of concentrated fishing activity 16 , combined with the threat posed by extrinsic disturbances such as cyclones, outbreaks of crown-of-thorns starfish and mass coral bleaching 15,17,18 . The WAMAFMF is the second largest coral fishery. ...
Full-text available
Coral reefs are highly threatened environs subject to ongoing unprecedented degradation as a result of anthropogenic activities. Given the existential threat to coral reef ecosystems, extractive industries that make use of coral reef resources, are facing significant public and political pressure to quantify and justify their environmental impact. In Australia, hundreds of thousands of live scleractinian (hard) corals are harvested annually directly from the wild to supply the growing international marine aquarium trade. Many of the most popular and high value aquarium corals are believed to be slow growing, which would make them particularly vulnerable to over-fishing. Corals present a number of unique challenges for fisheries management, not least of which, is the marked variation in the size of corals, which may be harvested in whole or in part. This issue is further compounded because harvest limits are typically weight-based, but there is very limited information on the standing biomass of corals in targeted stocks. Herein, we describe size-weight relationships for some of Australia’s most heavily targeted coral species ( Catalaphyllia jardinei , Duncanopsammia axifuga , Euphyllia glabrescens , Homophyllia cf. australis , Micromussa lordhowensis , Trachyphyllia geoffroyi ), which allows estimation of standing biomass from transect surveys. This work represents an important first step in the development of ecologically sound management strategies by bridging the gap between catch reporting and stock assessments.
... Others went further to explore the causes of recent decline and decreased resilience of corals on the Great Barrier Reef, identifying the negative impacts of chronic heat stress and bleaching events (Ceccarelli et al., 2020;MacNeil et al., 2019;Osborne et al., 2017;Pisapia et al., 2019). Another subset of these papers explored projections of future scenarios through both laboratory experiments (Dove et al., 2013;Pratchett et al., 2020) and simulations (Descombes et al., 2015) with a focus on coral decalcification, bleaching, and mortality. This warming-inducted decline in coral was linked to negative flow-on ecological effects on fish populations (Holbrook et al., 2015) and incidence of coral disease (Maynard et al., 2011), as well as negative economic and social effects associated with loss of fisheries revenue and shoreline protection (Pendleton et al., 2016) and "Reef Grief", or feelings of loss and mourning associated with coral bleaching and mortality on the Great Barrier Reef (Marshall et al., 2019). ...
Oceans and coasts provide important ecosystem, livelihood, and cultural values to humans and the planet but face current and future compounding threats from anthropogenic activities associated with expanding populations and their use of and reliance on these environments. To respond to and mitigate these threats, there is a need to first systematically understand and categorise them. This paper reviewed 226 articles from the period 2010–2020 on threats to Australia's oceans and coasts, resulting in the identification of a total of 307 threats. Threats were grouped into three broad categories — threats from use and extraction; environmental and human-induced threats; and policy and socio-political threats —then ranked by frequency. The most common ‘threats from use and extraction’ were recreational activities, non-point source pollution, and urban development; the most common ‘environmental and human-induced threat’ was increased temperatures; and the most common ‘policy and socio-political threat’ was policy gaps and failures (e.g., a lack of coastal climate adaptation policies). The identification of threats across all three categories increased over time; however, the identification of ‘threats from use and extraction’ increased most rapidly over the last four years (2017–2020). Threats were most often described for their impacts on environmental values (68%), followed by economic (14%), socio-cultural (12%), and Indigenous (6%) values. Only 45 of the 226 papers (20%) discussed multiple threats. The threats facing Australia's oceans and coasts are rising, cumulative, and multi-faceted, and the inherent tensions between varied uses, along with intensification of uses that derive short-term anthropogenic benefit, will continue to degrade the ecological sustainability of ocean and coastal systems if actions are not taken.
Full-text available
Duncanopsammia axifuga (Scleractinia: Dendrophylliidae) is reported for the first time from Indonesia. A population was found in 5-m deep, murky water on a sediment-rich, inshore reef at Bird’s Head Peninsula, West Papua. Some corals were attached to dead coral and others were loose fragments living on sediment. One attached specimen was observed to be damaged as a result of direct contact with an adjacent Goniopora coral. Free-living specimens on sand are more likely able to escape competition for space. These observations may help to better understand the northernmost range limit and the natural environment of D. axifuga, a species that is popular in the international aquarium trade, but has not been studied very well in the field.
Full-text available
The 2014–2017 Global Coral Bleaching Event is the longest, most widespread, and impactful on record. Rapid ecological assessment surveys by NOAA’s Pacific Reef Assessment and Monitoring Program reported widespread coral mortality at Jarvis Island in the aftermath of the 2015–2016 super-El Niño warming event; hard coral cover declined from 18.7% in April 2015 (pre-bleaching) to 0.4% in May 2016 (post-bleaching), representing a catastrophic > 98% decline. Between 2015 and 2016, corals at Jarvis experienced maximum heat stress of 22.25 °C-weeks exceeding the bleaching threshold (28.72 °C) for 66 consecutive weeks. Mass coral bleaching was observed in November 2015, which resulted in mass mortality across all coral taxa, depths, and island sectors. The bleaching event altered the benthic community composition including the coral assemblage. In the 2 yrs post-bleaching, the benthic community has transitioned from a short-lived increase of encrusting macroalgae to a more recent near-recovery of crustose coralline algae. Coral cover had not recovered by 2017 and could be potentially delayed by fast-growing turf algae. Within the coral community, the pre-bleaching dominant genus Montipora exhibited extreme mortality and only a handful of colonies of this taxon were enumerated in the 2016 surveys and none in 2017. Some coral taxa have persisted in low densities, including the ESA-threatened Acropora retusa and colonies of encrusting Pavona, Psammocora, and the free living Fungia. As the frequency and intensity of these high-temperature events is projected to increase in coming years, it is essential to track how remote ecosystems normally undisturbed by human influence, such as Jarvis, respond to a climate change.
Full-text available
The reefs of Guam, a high island in the Western Pacific, were impacted by an unprecedented succession of extreme environmental events beginning in 2013. Elevated SSTs induced severe island-wide bleaching in 2013, 2014, 2016, and 2017. Additionally, a major ENSO event triggered extreme low tides beginning in 2014 and extending through 2015, causing additional coral mortality from subaerial exposure on shallow reef flat platforms. Here, we present the results of preliminary analyses of environmental and biological data collected during each of these events. Accumulated heat stress in 2013 was the highest since satellite measurements began, but this record was exceeded in 2017. Overall, live coral cover declined by 37% at shallow reef flat sites along the western coast, and by 34% at shallow seaward slope sites around the island. Staghorn Acropora communities lost an estimated 36% live coral cover by 2017. Shallow seaward slope communities along the eastern windward coast were particularly devastated, with an estimated 60% of live coral cover lost between 2013 and 2017. Preliminary evidence suggests that some coral species are at high risk of extirpation from Guam’s waters. In light of predictions of the near-future onset of severe annual bleaching, and the possibility that the events of 2013–2017 may signal the early arrival of these conditions, the persistence of Guam’s current reef assemblages is in question. Here, we present detailed documentation of ongoing changes to community structure and the status of vulnerable reef taxa, as well as a critical assessment of our response protocol, which evolved annually as bleaching events unfolded. Such documentation and analysis are critical to formulating effective management strategies for the conservation of remaining reef diversity and function.
Full-text available
Understanding pressure pathways and their cumulative impacts is critical for developing effective environmental policy. For coral reefs, wide spread bleaching resulting from global warming is occurring concurrently with local pressures, such as increases in suspended sediments through coastal development. Here we examine the relative importance of suspended sediment pressure pathways for dredging impacts on corals and evidence for synergistic or antagonistic cumulative effects between suspended sediments and thermal stress. We show that low to moderate reductions in available light associated with dredging may lead to weak antagonistic (less than expected independently) cumulative effects. However, when sediment loads are high any reductions in mortality associated with reduced bleaching are outweighed by increased mortality associated with severe low light periods and high levels of sediment deposition and impacts become synergistic (greater than what would occur independently). The findings suggest efforts to assess global cumulative impacts need to consider how pressures interact to impact ecosystems, and that the cumulative outcome may vary across the range of realised pressure fields.
Full-text available
The global coral bleaching event of 2014-2017 resulted from the latest in a series of heat stress events that have increased in intensity. We assessed global-and basin-scale variations in sea surface temperature-based heat stress products for 1985-2017 to provide the context for how heat stress during 2014-2017 compared with the past 3 decades. Previously, undefined ''Heat Stress Year'' periods (used to describe interannual variation in heat stress) were identified for the Northern and Southern Hemispheres, in which heat stress peaks during or shortly after the boreal and austral summers, respectively. The proportion of reef pixels experiencing bleaching-level heat stress increased through the record, accelerating during the last decade. This increase in accumulated heat stress at a bleaching level is a result of longer stress events rather than an increase in the peak stress intensity. Thresholds of heat stress extent for the three tropical ocean basins were established to designate ''global'' events, and a Global Bleaching Index was defined that relates heat stress extent to that observed in 1998. Notably, during the 2014-2017 global bleaching event, more than three times as many reefs were exposed to bleaching-level heat stress as in the 1998 global bleaching.
Full-text available
Western Australia’s coral reefs have largely escaped the chronic pressures affecting other reefs around the world, but are regularly affected by seasonal storms and cyclones, and increasingly by heat stress and coral bleaching. Reef systems north of 18°S have been impacted by heat stress and coral bleaching during strong El Niño phases and those further south during strong La Niña phases. Cumulative heat stress and the extent of bleaching throughout the northern reefs in 2016 were higher than at any other time on record. To assess the changing regime of disturbance to reef systems across Western Australia (WA), we linked their site-specific exposure to damaging waves and heat stress since 1990 with mean changes in coral cover. Since 2010, there has been a noticeable increase in heat stress and coral bleaching across WA. Over half the reef systems have been severely impacted by coral bleaching since 2010, which was further compounded by cyclones at some reefs. For most (75%) reef systems with long-term data (5–26 yrs), mean coral cover is currently at (or near) the lowest on record and a full recovery is unlikely if disturbances continue to intensify with climate change. However, some reefs have not yet experienced severe bleaching and their coral cover has remained relatively stable or increased in recent years. Additionally, within all reef systems the condition of communities and their exposure to disturbances varied spatially. Identifying the communities least susceptible to future disturbances and linking them through networks of protected areas, based on patterns of larval connectivity, are important research and management priorities in coming years while the causes of climate change are addressed.
Full-text available
Between 2014 and 2017, an unprecedented heat stress accumulated and propagated across the tropical oceans and resulted in the so-called Third Global Bleaching Event (TGBE). Information about the effects of the TGBE in marginal coral reef provinces are still scarce, but can be relevant to understand the trajectories of coral reefs as climate changes intensify. Akin to deep mesophotic reefs and reefs in thermally stressed regions, low diversity, turbid-zone reefs may exhibit high bleaching tolerance due to local adaptations and conditions (e.g., shading by turbidity). Here, we summarize previous bleaching events in the tropical Western South Atlantic Ocean and explore taxonomic, cross-shelf and habitat-related bleaching trends in the Abrolhos reefs in February, May, June and October 2016, and March 2017. Fire corals (Millepora spp.) were the most affected, but all scleractinian species and several octocorals and zoanthids also bleached. Bleaching prevalence was higher in shallow coastal and offshore reef arcs than in deeper mesophotic reefs. All coral species bleached, but there were taxonomic and habitat-related trends in bleaching prevalence. Several species bleached less in the sites and habitats where their abundance was lower. As of March 2017, coral mortality was overall low across the region (< 3% of total coral cover). Our results add to the recent evidence that deep reefs provide partial refugia for a few coral species, and that turbid-zone reefs may be less susceptible to climate stress due to shading, higher heterotrophy levels, and local adaptations.
Full-text available
Coral reefs of the Persian/Arabian Gulf were the last to succumb to the effects of the global-scale mass coral bleaching event that began in 2015. This study examines the causes and consequences of the 2017 bleaching event on eight reefs located across > 350 km of the southern basin of the Gulf. Using a combination of 5 yr (2013–2017) of reef-based temperature observations, local meteorological data and water column modeling, we show that 2017 was characterized by an extended period of mid-summer calm when winds rarely exceeded breeze conditions, reducing evaporative heat loss and inducing dramatic warming compared with non-bleaching years (2013–2016). Reef-bottom temperatures in the Gulf in 2017 were among the hottest on record, with mean daily maxima averaging 35.9 ± 0.1 °C across sites, with hourly temperatures reaching as high as 37.7 °C. Across the southern Gulf, corals spent nearly 2 months (mean 55.1 ± 3.9 d above bleaching temperatures and nearly 2 weeks above lethal temperatures (11.8 ± 2.4 d), substantially longer than in the non-bleaching years (2013–2016) and equating with 5.5 °C-weeks of thermal stress as degree heating weeks. As a result, 94.3% of corals bleached, and two-thirds of corals were lost to mortality between April and September 2017. Mortality continued after peak bleaching, and by April 2018 coral cover averaged just 7.5% across the southern basin, representing an overall loss of nearly three-quarters of coral (73%) in 1 yr. This mass mortality did not cause dramatic shifts in community composition as earlier bleaching events had removed most sensitive taxa. An exception was the already rare Acropora which were locally extirpated in summer 2017. Given the increasing frequency of mass bleaching in the Gulf and the above global rates of regional warming, the capacity for recovery and the prognosis for the future of Gulf reefs are not optimistic.
Full-text available
The frequency and duration of episodic ocean warming events are increasing, threatening the integrity of coral reefs globally. Interspecific differences in susceptibility to heat stress result from variable capacities of corals to resist bleaching or to persist in a bleached state. During shorter bleaching events, stress responses occur rapidly and the “window” for detecting bleaching is tightly constrained. However, during longer bleaching events, we argue that the timing of surveys can radically influence results, which need to be interpreted with care. For example, although “heat-resistant” corals may survive prolonged bleaching events, they have a greater chance of being recorded as having bleached because they can persist for longer in a bleached state. This could lead to erroneous conclusions about their vulnerability to heat stress compared with taxa that bleach and die rapidly. Therefore, as bleaching events lengthen, it is vital to consider not only temperature at the time of sampling, but also the accumulation of heat stress over the entire warming event. We present a simplified conceptual framework and an example from the Central Pacific to emphasize the importance of survey timing to perceived susceptibility of coral taxa to bleaching.
Full-text available
Considerable attention has been directed at understanding the consequences and impacts of long-term anthropogenic climate change. Discrete, climatically extreme events such as cyclones, floods, and heatwaves can also significantly affect regional environments and species, including humans. Climate change is expected to intensify these events and thus exacerbate their effects. Climatic extremes also occur in the ocean, and recent decades have seen many high-impact marine heatwaves (MHWs)—anomalously warm water events that may last many months and extend over thousands of square kilometers. A range of biological, economic, and political impacts have been associated with the more intense MHWs, and measuring the severity of these phenomena is becoming more important. Progress in understanding and public awareness will be facilitated by consistent description of these events. Here, we propose a detailed categorization scheme for MHWs that builds on a recently published classification, combining elements from schemes that describe atmospheric heatwaves and hurricanes. Category I, II, III, and IV MHWs are defined based on the degree to which temperatures exceed the local climatology and illustrated for 10 MHWs. While there is a long-term increase in the occurrence frequency of all MHW categories, the largest trend is a 24% increase in the area of the ocean where strong (Category II) MHWs occur. Use of this scheme can help explain why biological impacts associated with different MHWs can vary widely and provides a consistent way to compare events. We also propose a simple naming convention based on geography and year that would further enhance scientific and public awareness of these marine events.
Global warming and overexploitation both threaten the integrity and resilience of marine ecosystems. Many calls have been made to at least partially offset climate change impacts through local conservation management. However, a mechanistic understanding of the interactions of multiple stressors is generally lacking for habitat‐forming species; preventing the development of sound conservation strategies. We examined the effectiveness of no‐take marine protected areas ( MPA s) at enhancing structural complexity and resilience to climate change on populations of an overexploited and long‐lived octocoral. We used long‐term data over eight populations, subjected to varying levels of disturbances, and Integral Projection Models to understand how the overfishing and mass‐mortality events shape the stochastic dynamics of the Mediterranean red coral Corallium rubrum . Marine protected areas largely reduced colony partial mortality (i.e. shrinkage), enhancing the structural complexity of coral populations. However, there were no significant differences in individual mortality or population growth rates between protected and exploited populations. In contrast, warming had detrimental consequences for the long‐term viability of red coral populations, driving steady declines and potential local extinctions due to sharp effects in survival rates. Stochastic demographic models revealed only a weak compensatory effect of MPA s on the impacts of warming. Policy implications . Our results suggest that marine protected areas ( MPA s) are an effective local conservation tool for enhancing the structural complexity of red coral populations. However, MPA s may not be enough to ensure red coral's persistence under future increases in thermal stress. Accordingly, conservation strategies aiming to ensure the persistence and functional role of red coral populations should include management actions at both local (well‐enforced MPA s) and global scales (reductions in greenhouse gas emissions). Finally, this study unravels the divergent demographic consequences that can arise from multiple stressors and highlights the key role of demography in better understanding and predicting the consequences of combined impacts for vulnerable ecosystems.