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Shifting communities after typhoon damage on an upper mesophotic reef in Okinawa, Japan



Very few studies have been conducted on the long-term effects of typhoon damage on mesophotic coral reefs. This study investigates the long-term community dynamics of damage from Typhoon 17 (Jelawat) in 2012 on the coral community of the upper mesophotic Ryugu Reef in Okinawa, Japan. A shift from foliose to bushy coral morphologies between December 2012 and August 2015 was documented, especially on the area of the reef that was previously recorded to be poor in scleractinian genera diversity and dominated by foliose corals. An area with higher diversity of scleractinian coral genera was observed to be less affected by typhoon damage with more stable community structure due to less change in dominant coral morphologies. Despite some changes in the composition of dominant genera, the generally high coverage of the mesophotic coral community is facilitating the recovery of Ryugu Reef after typhoon damage.
Submitted 26 March 2017
Accepted 22 June 2017
Published 18 August 2017
Corresponding author
Kristine N. White,,
Academic editor
Robert Toonen
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DOI 10.7717/peerj.3573
2017 White et al.
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Shifting communities after typhoon
damage on an upper mesophotic reef in
Okinawa, Japan
Kristine N. White1,*, David K. Weinstein2,*, Taku Ohara2,3, Vianney Denis4,
Javier Montenegro2,5and James D. Reimer2,5
1Department of Biology, The University of Tampa, Tampa, FL, United States of America
2Graduate School of Engineering and Science, University of the Ryukyus, Nishihara, Okinawa, Japan
3Benthos Divers, Onna, Okinawa, Japan
4Institute of Oceanography, National Taiwan University, Taipei, Taiwan
5Tropical Biosphere Research Center, University of the Ryukyus, Nishihara, Okinawa, Japan
*These authors contributed equally to this work.
Very few studies have been conducted on the long-term effects of typhoon damage on
mesophotic coral reefs. This study investigates the long-term community dynamics of
damage from Typhoon 17 (Jelawat) in 2012 on the coral community of the upper
mesophotic Ryugu Reef in Okinawa, Japan. A shift from foliose to bushy coral
morphologies between December 2012 and August 2015 was documented, especially
on the area of the reef that was previously recorded to be poor in scleractinian genera
diversity and dominated by foliose corals. Comparatively, an area with higher diversity
of scleractinian coral genera was observed to be less affected by typhoon damage with
more stable community structure due to less change in dominant coral morphologies.
Despite some changes in the composition of dominant genera, the generally high
coverage of the mesophotic coral community is facilitating the recovery of Ryugu Reef
after typhoon damage.
Subjects Biodiversity, Ecology, Marine Biology, Biosphere Interactions, Natural Resource
Keywords Mesophotic, Succession, Coral reef, Pachyseris, Japan, Typhoon recovery, Shifting
Scleractinian corals are the primary architects of reef ecosystems and the major contributors
to reef rugosity, a fundamental parameter for the resilience of the ecosystem after a
disturbance (Graham et al., 2015). Therefore, documenting the extent of damage to
corals after perturbations is key to understanding the potential trajectory of recovery.
To quantify the shifts in functional composition of coral reefs after environmental and
anthropogenic disturbances, Darling et al. (2012) determined coral life history strategies
based on several traits, including growth form, reproductive mode, and fecundity. Shifts
to stress-tolerant, generalist and weedy species after disturbances have been documented
in both the Caribbean (Alvarez-Filip et al., 2009;Alvarez-Filip et al., 2011) and the Indo-
Pacific (McClanahan et al., 2007;Rachello-Dolmen & Cleary, 2007). Recruitment of coral
How to cite this article White et al. (2017), Shifting communities after typhoon damage on an upper mesophotic reef in Okinawa, Japan.
PeerJ 5:e3573; DOI 10.7717/peerj.3573
larvae can be an important factor in the recovery of a coral reef (Pearson, 1981), but plays
a lesser role if there is regrowth from surviving coral colonies and/or if fragmentation
occurs (Hughes, 1985). Shallow areas with few local survivors are most likely dependent on
recruitment and show low rates of recovery, whereas areas with many survivors often show
rapid recovery due to regrowth of remnant colonies (Connell, Hughes & Wallace, 1997).
The recovery of coral reefs after disturbances is usually measured by changes in coral
cover, abundance, species composition, and/or diversity (Davis, 1982;Connell, Hughes &
Wallace, 1997;Graham et al., 2015). The type of disturbance, original species composition,
reef complexity (rugosity), and depth are all thought to be responsible for the wide
variation in patterns of recovery. For example, a 95-year study of Dry Tortugas Reef in
Florida demonstrated a relatively constant abundance of coral and other benthic organisms,
despite changes in species composition and coral reef structure (Davis, 1982). However, if
coral cover is significantly reduced after a disturbance, the reef will likely undergo a shift in
the composition of coral species to the coral species that survived the disturbance (Connell,
Hughes & Wallace, 1997), or to other taxa, such as fleshy macroalgae. For example, phase
shifts from scleractinian coral dominance to fleshy macroalgae were observed after multiple
storm and anthropogenic disturbances on Jamaican reefs over 40 years (Hughes, 1994).
Reports measuring coral reef recovery after storm disturbances based on coral cover on
shallow reefs vary in time from two to 15 years, with little attention paid to species
composition (Pearson, 1981;Platt & Connell, 2003;Gardner et al., 2005). Ecological
succession (the replacement of early species with late species; Cowles, 1899) occurs
following disturbances, and community recovery processes are affected by different types of
disturbances that create the opportunity for a change in succession (Platt & Connell, 2003).
Storms often result in various successional states or phase shifts, for which the capacity to
return to the original condition has been intensively debated (Dudgeon et al., 2010;Bruno,
2014;Dixon et al., 2015). Coral cover throughout Caribbean coral reefs decreased by an
average of 17% after hurricanes between 1980 and 2001, with no further coral loss in the
year following a disturbance and no evidence of recovery eight years after a disturbance
(Gardner et al., 2005). Gardner et al. (2005) suggested that the lack of recovery was a result
of other stressors such as sedimentation or eutrophication impacting shallow reefs and
that exposure to storms makes coral reefs less susceptible to storms in the future due to the
recovery of more tolerant species.
Most coral reef storm recovery studies have been conducted on relatively shallow
Caribbean reefs (e.g., Stoddart, 1974;Shinn, 1976;Pearson, 1981), but more work is needed
to understand storm recovery on Indo-Pacific reefs in general and mesophotic reefs
in particular. In one example from the Indo-Pacific, coral cover on a 6–12 m tabulate
Acropora reef in the Coral Sea declined from 80% to less than 10% after several storms
over a two year period, leaving only encrusting and robust coral species (Halford et al.,
2004). This was followed by coral cover increasing exponentially 5–9 years after the storm
disturbances, with the reef having recovered to pre-storm levels after 11 years, albeit with
a shift from branching to tabulate coral morphology (Halford et al., 2004). In another
example, Nozawa, Lin & Chung (2013) examined coral recruitment at 5 and 15 m depths
in Taiwan, and concluded that shallower coral reefs with more pocilloporid and poritid
White et al. (2017), PeerJ , DOI 10.7717/peerj.3573 2/15
recruits were more influenced by post-settlement processes compared to deeper reefs that
have more acroporid recruits and were more affected by pre-settlement processes.
Unlike their shallow-water counterparts, there is very little information available
documenting recovery of mesophotic coral reefs (benthic communities including
hermatypic zooxanthellate corals at 30–150 m depths (Baker, Puglise & Harris, 2016))
after storm disturbances. Although it has often been assumed that mesophotic reefs are
relatively protected from storm damage (Bongaerts et al., 2010), recent studies have shown
this is not the case (Bongaerts, Muir & Bridge, 2013;White et al., 2013). The impact of
storms on patterns of benthic communities documented on large horizontal scales can
help to determine upper mesophotic shelf edge (30–60 m) coral development (Smith et al.,
2016). Depending on the topography and distance between shallow and deep reefs, storms
can damage corals on low-angle slopes as a result of coral debris or sediment transported
down the reef slope compared to high-angle slopes (Bongaerts et al., 2010); whereas other
low-angle upper mesophotic reefs do not appear to be impacted by terrestrial sediment
transport (Weinstein, Klaus & Smith, 2015). Growth rates of different coral species may
also be a factor in recovery processes (Bongaerts et al., 2015). Studies suggest that upper
mesophotic coral species in the Caribbean have comparatively slower growth rates than
shallow water coral species (Dustan, 1975;Hughes & Jackson, 1985;Leichter & Genovese,
2006;Weinstein et al., 2016). However, Bongaerts et al. (2015) reported that growth rates
of some coral species at lower mesophotic depths (60–150 m) may be similar to observed
rates in shallow water.
One of the few ecological studies monitoring the direct impact of storm damage on
a mesophotic reef system is from Okinawa, Japan. Ohara et al. (2013) described Ryugu
Reef as an upper mesophotic reef with a large, nearly monospecific stand of Pachyseris
foliosa from 32 to 45 m. Heading deeper, away from shore, Ryugu Reef transitions on a
low-angle slope from rubble with some corals (Fungiidae) at 21 m; to a high diversity of
corals at 26 m; a Pachyseris- dominated area at 31 m; and finally to sand at 42 m. The
center of Typhoon 17 (Jelawat), the strongest typhoon ever recorded to hit Okinawa-jima
Island, with wave heights up to 12 m, passed within 30 km of Ryugu Reef on 29 September
2012 (Ohara et al., 2013;White et al., 2013). Analyses of coral species composition and
morpho-functional groups on Ryugu Reef before and after Typhoon 17 suggested that the
highly diverse areas were less susceptible to typhoon damage (White et al., 2013). White et
al. (2013) also theorized that Ryugu Reef would be resilient because of a high likelihood
of recovery based on only slight changes in functional groups after the typhoon. Despite
such speculation, little is known regarding long-term recovery of mesophotic reef systems
following major storm events.
Previous studies suggest that coral communities recover from storm disturbances via
succession (Gardner et al., 2005;McClanahan et al., 2007;Rachello-Dolmen & Cleary, 2007;
Alvarez-Filip et al., 2009;Alvarez-Filip et al., 2011;Hughes et al., 2012;Smith et al., 2016),
with dominant coral genera shifting until the reef can mature and possibly return to initial
conditions (Dudgeon et al., 2010;Bruno, 2014). Halford et al. (2004) observed exponential
coral growth on the southern Great Barrier Reef 5–9 years after storms. Signs of recovery
were documented on the Great Barrier Reef as early as 24–35 months after Tropical
White et al. (2017), PeerJ , DOI 10.7717/peerj.3573 3/15
Cyclone Yasi in 2011, with evidence of regrowth of branching corals on King Reef (Perry
et al., 2014) and an average 4% increase in coral cover on 19 reefs in the Great Barrier Reef
Marine Preserve (Beeden et al., 2015). Combined, these results suggest that Indo-Pacific
reefs’ successional changes may occur only a few years after a storm event. Thus, the
objectives of this study include documenting the initial recovery of an upper mesophotic
coral reef (Ryugu Reef) over a four-year period (2012–2015), and describing resulting
changes in scleractinian coral communities based on functional morphology and species
composition. This study provides the first in-depth record of an upper mesophotic reef
shifting communities based on functional group changes after a storm disturbance and
offers insight into the implications of this shift in the recovery of mesophotic coral reefs.
Random line transects were surveyed at Ryugu Reef (see map of stations in Fig. 1B; White
et al., 2013) at seven locations near station 2 (30–32 m) and seven locations near station 3
(26–30 m). Adjacent 4×6 cm2photographs (12–79 per transect) were taken along a 10-m
tape for each line transect 1.5 years after Typhoon 17 (designated ‘2014’ dataset) and 2.5–3
years after the typhoon (designated ‘2015’ dataset). Scleractinian coral (+one Millepora
sp., hereafter ‘coral’) operational taxonomic units (OTUs) were identified in a similar
manner as in White et al. (2013), following Hoeksema (1989) and Gittenberger, Reijnen &
Hoeksema (2011) for Fungiidae, Huang et al. (2016) for Lobophylliidae, Huang et al. (2014)
for Merulinidae, Diploastraeidae and Montastraeidae, and Veron (2000) for all remaining
corals. Scientific binomens were checked for validity in the World Register of Marine Species
(WoRMS; Hoeksema & Cairns, 2015; accessed May 2, 2017). Post-typhoon data from 2012
(White et al., 2013) were combined with the newest dataset. Many mesophotic coral species
at Ryugu, particularly those within genera Acropora (see Wallace, 1999), Galaxea, and
Montipora, were very hard to conclusively identify to species level. Therefore, changes
in the community were investigated at the genus-level. Bray-Curtis dissimilarities were
calculated on raw data by comparing each transect to every other transect, and visualized
using non-metric multidimensional scaling (nMDS). Time-period centroids (spatial
median) were overlaid to visualize temporal dynamics. Differences in the composition
of the benthic assemblage between stations, and between temporal dynamics within each
station were tested using permutational multivariate analysis of variance (ADONIS).
Each coral OTU was described following similar methods to those described in
Denis et al. (2013) and White et al. (2013). Corals were assigned to one or more of eight
morphological groups as in White et al. (2013), following growth form information found
in Wallace (1999),Veron (2000),Pillay (2002) and Bellwood et al. (2004) as well as by
confirming morphologies from in situ photographs. OTU categories (massive/submassive,
encrusting, laminar/foliose, columnar, plate-like, bushy, arborescent and unattached
morphologies) are provided in Table S1. Often, colonies presented more than one
growth form in the field, and these OTUs were therefore assigned to two growth forms.
Community-level Weighted Means (CWM) of trait values (Lavorel et al., 2008) were
computed for each transect, and standardized to determine the relative contribution of
White et al. (2017), PeerJ , DOI 10.7717/peerj.3573 4/15
each morpho-functional group to the coral assemblage (removing all non-coral OTUs).
Contribution of a given morpho-functional group was summarized for each station/period
sampled and compared among years using Kruskal-Wallis tests followed by Conover’s
multiple comparison tests.
All data were analyzed in R v3.2.3 (R Core Team, 2014) using the packages Vegan
(Oksanen et al., 2016) and FD (Laliberté & Legendre, 2010;Laliberté, Legendre & Shipley,
Relative live coral cover increased at each station by 5% between 2012 and 2014 and by
another 6% between 2014 and 2015 (Table 1). Significant changes in cover of coral genera
occurred over time at both stations 2 and 3 (ADONIS test, R2=0.19, p<0.001) (Fig. 1).
However, variation between stations (ADONIS test, R2=0.41, p<0.001) was greater than
among years (Fig. 1). Station 3 showed minor changes in cover of coral genera between
2014 and 2015 after a major shift in coral assemblage between 2012 and 2014. Station
2 showed diversification of coral genera in the three years after Typhoon 17 (Jelawat)
with a decrease in Pachyseris cover and an increase in several other genera (Table 1). An
increase in cover of bushy corals (Acropora,Porites,Seriatopora,Stylophora) was significant
(Kruskal-Wallis/Conover tests, p<0.01) at station 3 as of 2015, compared to 2012 before
the typhoon (Fig. 2). Significant coral cover changes at station 2 as of 2015 included a
decrease of foliose corals, compared to 2012 before the typhoon (Kruskal-Wallis/Conover
test, p<0.05), an increase of bushy corals (Kruskal-Wallis/Conover test, p<0.01), and
an increase in some plate-like corals (p<0.05) (Fig. 2). A major factor in the decrease
of foliose coral cover at station 2 was the continuous decrease of Pachyseris from 2012
(post-typhoon) to 2015 (Table 1).
Percent cover of coral rubble/coralline algae decreased from 31% to 27% at station 2
between 2012b and 2014 from 27% to 7% between 2014 and 2015 (Table 1). This followed
a 29% increase in coral rubble/coralline algae directly after typhoon Jelawat (White et al.,
2013). At station 3, coral rubble/coralline algae decreased from 49% to 32% between 2012b
and 2014 and from 32% to 22% between 2014 and 2015.
Data are sparse on the recolonization of mesophotic reefs. The diversification of mesophotic
coral reef organisms after a disturbance may occur as a result of horizontal connectivity
with other mesophotic reefs or vertical connectivity with shallow water reefs (Kahng, Copus
& Wagner, 2014). Species with wide depth ranges are more likely to benefit from vertical
connectivity, while horizontal connectivity would most likely affect only the acquisition
of symbiotic zooxanthellae for species that acquire Symbiodinium from the water column
(Bongaerts et al., 2010;Kahng, Copus & Wagner, 2014). Over a short time, it is likely that
a storm disturbance would open up space in the area previously documented with nearly
100% Pachyseris coverage (Ohara et al., 2013), allowing more opportunistic species a
chance to prosper. Station 2 showed a diversification of coral species in the three years
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Table 1 Relative percent coral. Relative percent cover of coral genera, coral rubble/coralline algae, and pavement at stations 2 and 3 over time after
Typhoon Jelawat, 2012–2015.
Taxonomic units Station 2 (%) Station 3 (%)
December 2012 April 2014 March 2015 December 2012 April 2014 August 2015
Acropora <1 9 17 2 11 18
Agaraciidae 0 <1 <1 0 0 0
Astreopora 0 0 <1 0 <1 <1
Australomussa 0 0 <1 <1 <1 0
Caulastrea 0 0 0 0 <1 <1
Ctenactis <1 <1 <1 2 2 3
Danafungia <1 2 2 2 3 2
Dipsastraea 0 0 0 <1 0 <1
Echinophyllia <1 <1 <1 4 <1 <1
Euphyllia 0 0 <1 <1 <1 <1
Favites 0 0 0 <1 0 0
Galaxea 2 5 10 10 12 8
Halomitra 0 0 <1 <1 <1 0
Herpolitha 0 <1 <1 1 1 1
Lithophyllon 2 2 1 19 10 12
Lobophyllia 0 0 0 <1 0 0
Merulina 0 0 <1 0 <1 1
Montipora 0 <1 2 0 <1 4
Mycedium 0 <1 1 <1 1 1
Oxypora 0 <1 <1 0 <1 0
Pachyseris 58 49 34 3 4 4
Pavona 0 0 <1 4 <1 2
Pectinia 0 0 <1 0 <1 <1
Pectiniidae 0 0 0 0 3 0
Pleuractis <1 1 1 1 3 3
Porites 0 <1 <1 <1 <1 <1
Seriatopora 0 <1 <1 0 <1 0
Stylophora 0 0 <1 0 <1 <1
Turbinaria 0 0 0 <1 0 0
Coral rubble/coralline algae 37 21 7 49 32 22
Pavement N/A 11 19 N/A 12 16
Unknown live coral 0 <1 <1 <1 1 1
Total live coral cover 63 68 74 51 56 62
after Typhoon 17 (Jelawat) created vacant ecological niches (Table 1). Pachyseris (foliose
morphology) cover decreased immediately following the typhoon (White et al., 2013),
allowing the increased growth of arborescent, bushy, columnar, massive, and encrusting
morphologies (Fig. 3), although significant increases were only seen in bushy genera at
this station (Kruskal-Wallis/Conover test, p<0.01). At least six of the ‘massive’ genera
(Astreopora,Caulastrea,Favites,Galaxea,Goniastrea,Plerogyra) have been noted to be
‘stress-tolerant’ and four ‘weedy’ genera (fast growing with high turnover) are known
White et al. (2017), PeerJ , DOI 10.7717/peerj.3573 6/15
−1 0 1
−1.0 −0.5 0.0 0.5 1.0
NMDS Axis 1
NMDS Axis 2
station 2
station 3
Plerogyra P
Unknown hard coral
Noncoral organism
Unknown Fungidae
nknown Fu
Coralline algae/Coral rubble
Figure 1 nMDS genus data. nMDS genus data with stress value of 0.16. Station factor (Bray-Curtis
dissimilarities test, R2=0.41, p<0.001); temporal factor (Bray-Curtis dissimilarities test, R2=0.19,
p<0.001). 2012A refers to pre-typhoon data and 2012B refers to post-typhoon data, both from
White et al. (2013).
to do well under disturbance (Goniastrea, Porites,Seriatopora,Stylophora) (Darling et al.,
2012). However, the dominant genus (Pachyseris) on Ryugu Reef is a ‘generalist’ (Darling
et al., 2012). It appears that Typhoon Jelawat created the opportunity for genera aside from
Pachyseris to increase coverage, and these genera could possibly consist of opportunistic
species at upper mesophotic depths. Similarly, areas of the Great Barrier Reef recovered at
different rates after disturbances, with the fastest recovery rates occurring when more space
was available as a result of reduced coral cover (Graham et al., 2014). At Ryugu Reef, coral
rubble cover decreased from the post-typhoon survey of 2012 (Table 1), and Pachyseris
coral cover continually decreased in the four years post-typhoon. Following damages
from the typhoon, diversification of the area previously dominated by Pachyseris corals
occurred, with an increase in cover of genera such as Seriatopora and Galaxea. It is possible
that colonies of these genera were previously present but in much smaller numbers than
Pachyseris or that these genera contain opportunistic species.
Immediately after Typhoon 17, little change in coral community assemblage was evident
at the shallower station 3, suggesting that the diverse/complex community was more
resistant due to lower impact on individual genera than the impact on the Pachyseris-
dominated community (White et al., 2013). At station 3, corals recovered with progressive
White et al. (2017), PeerJ , DOI 10.7717/peerj.3573 7/15
station 2
station 3
Relative contribution (% morphology)
2012A 2012B 2014 2015
2012A 2012B 2014 2015
C* G
Figure 2 Community weight mean (CWM) of trait values. Community weight mean (CWM) of trait
values representing the contribution (%) of corals representing each given morphology. Significant re-
sults are shaded with a grey background (Kruskal-Wallis/Conover tests, * p<0.05; *** p<0.01). 2012A
refers to pre-typhoon data and 2012B refers to post-typhoon data, both from White et al. (2013). (A) Ar-
borescent; (B) Plate-like; (C) Laminar & Foliose; (D) Massive & Submassive; (E) Bushy; (F) Columnar;
(G) Unattached; (H) Encrusting.
recolonization of the available substrate via surviving corals between 2012 (post-typhoon)
and 2015 (Table 1). Cover of Acropora,Ctenactis,Danafungia, Porites,Seriatopora, and
Stylophora increased, suggesting that bushy and unattached coral genera did better than
the foliose genera (Montipora,Mycedium,Oxypora,Pachyseris) that stabilized with no
significant increase or decrease in cover at station 3 (Table 1).
Major shifts in functional groups were evident at both stations 2 and 3 post-typhoon
(Fig. 1). Foliose genera decreased at stations 2 and 3 after the typhoon, with a significant
decrease as of 2015 at station 2 (Kruskal-Wallis/Conover test, p<0.05). These results are
similar to a previous shallow-water study on the Great Barrier Reef in which foliose coral
colonies declined drastically after a storm event (Perry et al., 2014). Bushy coral genera
increased at both Ryugu stations post-typhoon (Kruskal-Wallis/Conover test, p<0.01).
The functional shift shows that beyond the apparent recovery of Ryugu Reef, the trajectory
followed could lead ultimately to a fundamentally different coral community, as previously
reported from the Great Barrier Reef (Harmelin-Vivien, 1994). However, maturation of
White et al. (2017), PeerJ , DOI 10.7717/peerj.3573 8/15
Figure 3 Station 2. Example of community shift from foliose to bushy coral genera on Ryugu Reef at sta-
tion 2 (30–32 m) from (A) 2012 (pre-typhoon); (B) 2012 (post-typhoon); (C) 2014; and (D) 2015.
the coral assemblage with time may lead to the return of a state dominated by generalist
Pachyseris corals (Darling et al., 2012). Continued monitoring of Ryugu Reef will determine
whether this community will return to the initial state recorded prior to Typhoon 17 or if
eventually the ecosystem might reach stability in an alternative configuration.
White et al. (2013) hypothesized that mesophotic reefs such as Ryugu would be resilient
and recover quickly after disturbance to the original conditions of the reef. The current
data do not support this hypothesis as a shift in community structure to more bushy and
columnar morphologies and less foliose morphologies was observed. The large Pachyseris
stand at station 2 was heavily damaged after Typhoon 17 (Jelawat) in 2012, but showed
signs of recovery in 2015 with only slight diversification of the coral community. This
fast recovery, combined with behavioral characteristics, may enable Pachyseris spp. to
outcompete other coral genera at upper mesophotic depths, allowing Ryugu Reef to
return to the initial, pre-typhoon coral assemblage. However, if Ryugu Reef coral genera
are limited by their growth rates as many other mesophotic coral genera are (Dustan,
1975;Hughes & Jackson, 1985;Leichter & Genovese, 2006;Weinstein et al., 2016), it is more
likely that there will be a permanent shift with increasing presence of weedy or stress-
tolerant species (McClanahan et al., 2007;Rachello-Dolmen & Cleary, 2007;Alvarez-Filip
et al., 2009;Hughes et al., 2012). While the dominant genera are changing on Ryugu Reef,
there were no new species recorded, suggesting the regrowth of damaged corals or local
recruitment. Examinations of shallow Acropora corals around Okinawa Main Island
(Shinzato et al., 2015) and on the Great Barrier Reef after Cyclone Yasi (Lukoschek et al.,
White et al. (2017), PeerJ , DOI 10.7717/peerj.3573 9/15
2013) both suggest the importance of local recruitment for replenishment of Acropora
species, and such research remains to be conducted on corals of deeper reefs such as Ryugu
Reef. The high live coral cover of Ryugu Reef suggests that although mesophotic reefs
may be affected by large storms, recovery may be facilitated by the relative stability of the
mesophotic zone.
We thank boat captain Tokunobu Toyama for assistance in surveys. We also thank MISE lab
members I Kawamura, Y Kushida, V Nestor, T Kubomura, and H Kise, who assisted with
surveys. Dr. Z Richards (Western Australian Museum, Curtin University) is thanked for
advice on morpho-functional groups. Suggestions from Tom Bridge and Bert Hoeksema
improved an earlier version of this manuscript.
V Denis is the recipient of a grant from the Ministry of Science and Technology (Taiwan, no.
104-2611-M-002-020-MY2). JD Reimer was funded by a Japan Society for the Promotion
of Science (JSPS) ‘Zuno-Junkan’ grant entitled ‘‘Studies on origin and maintenance of
marine biodiversity and systematic conservation planning’’. D Weinstein was the recipient
of a JSPS short-term postdoctoral fellowship (PE14789). The funders had no role in study
design, data collection and analysis, decision to publish, or preparation of the manuscript.
Grant Disclosures
The following grant information was disclosed by the authors:
Ministry of Science and Technology: 104-2611-M-002-020-MY2.
Japan Society for the Promotion of Science (JSPS) ‘Zuno-Junkan’.
Studies on origin and maintenance of marine biodiversity and systematic conservation
JSPS short-term postdoctoral fellowship (PE14789).
Competing Interests
James D. Reimer is an Academic Editor for PeerJ. Taku Ohara is an employee of Benthos
Divers, Onna, Okinawa, Japan.
Author Contributions
Kristine N. White performed the experiments, analyzed the data, wrote the paper,
prepared figures and/or tables, reviewed drafts of the paper.
David K. Weinstein analyzed the data, wrote the paper, reviewed drafts of the paper.
Taku Ohara conceived and designed the experiments, performed the experiments,
contributed reagents/materials/analysis tools, reviewed drafts of the paper.
Vianney Denis analyzed the data, wrote the paper, prepared figures and/or tables,
reviewed drafts of the paper.
White et al. (2017), PeerJ , DOI 10.7717/peerj.3573 10/15
Javier Montenegro performed the experiments, prepared figures and/or tables, reviewed
drafts of the paper.
James D. Reimer conceived and designed the experiments, performed the experiments,
contributed reagents/materials/analysis tools, wrote the paper, reviewed drafts of the
Data Availability
The following information was supplied regarding data availability:
Data used for statistical analyses is uploaded as a Supplemental File.
Supplemental Information
Supplemental information for this article can be found online at
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... In recent years, more and more coral transplant bases and nurseries have been designed (Williams et al., 2019). The high mortality in most coral transplant experiments is caused by the dumping of the transplant carrier and the shedding of transplanted corals (White et al., 2017;Zheng et al., 2021). In the present study, the overall survival rate of 94.27% was significantly higher compared with the coral transplantation experiments conducted on Wuzhizhou Island by Zheng et al. (2021) and Zhang et al. (2021). ...
... In the present study, the overall survival rate of 94.27% was significantly higher compared with the coral transplantation experiments conducted on Wuzhizhou Island by Zheng et al. (2021) and Zhang et al. (2021). The reefs weighing 3 tons and a dense grid prevented a large number of coral deaths caused by the dumping of carriers and the shedding of corals (Lindahl, 2003;White et al., 2017;Zhang et al., 2016;Zheng et al., 2021). Beginning in August 2020, a significantly increased temperature in the South China Sea led to coral deaths, and transplanted corals in this area also showed increased mortality. ...
Due to climate change and human activities, coral reef ecosystems are facing a crisis of degradation globally. Some coral reefs in the northern part of Wuzhizhou Island (Southeastern Hainan Island, the South China Sea) have been fragmented because of continuous disturbance, and we systematically conducted in-situ restoration experiments to accelerate the ecological restoration in this area. In September 2019, 40 reefs with hollow structures were placed in the experimental area, and a control area was selected at the same depth. Twenty of the 40 reefs were covered by a cylindrical grid with a diameter of 0.5 cm (GFn group), and the remaining 20 were covered by a flat grid with a width of 1 cm (BFn group). A total of 1140 coral colonies, composed of Acropora hyacinthus, Acropora microphthalma, Acropora florida, Montipora truncata, and Porites lutea, were transplanted in this experiment, with an overall survival rate of 94.27% due to the coral transplant base of the carrying reefs being of sufficient weight, hollow structure, and dense grid. The survival rate and annual growth rate of Acropora in the GFn group with a narrow but large mesh and cylindrical design were significantly higher, and the fastest growth rate was found in A. hyacinthus, growing at 27.33 ± 10.37 cm²·month⁻¹. Montipora truncata and P. lutea in the BFn group with a wide mesh and flat structure had higher survival rates and significantly greater growth rates. In the ecology of the coral community, coral coverage in the GFn group was significantly higher compared with the BFn group, which was mainly attributed to the difference in the growth of Acropora. Compared with the reef fragmentation area, the three-dimensional structure of the hollow reef and its radiation effect significantly attracted the accumulation of large invertebrates and reef fishes. Sea cucumbers and sea urchins gathered faster, forming a stable community structure. The dominant fish species gradually transformed from the large algae-eating fish Siganus fuscessens to the territorial algae-eating fish Dascyllus reticulatus due to changes in the three-dimensional structure of the grid surface caused by coral growth. Studies have shown that the three-dimensional structure of a reef can significantly affect the aggregation of benthic organisms. Among the selected corals, Acropora grew more rapidly, which established more complex three-dimensional structures to achieve a better ecological restoration effect in the reef area. The combination of tiled Montipora and lumpy Porites could increase the base coverage and reduce the impact of algae on the corals. Our results suggest that when transplanting different types of corals, we should consider the use of multiple comprehensive factors such as the type of the reef, the structure of the grid, the characteristics of the transplanted corals, and the influence of environmental factors.
... In the last two and a half decades, however, coral reefs have confronted growing crises due to global climate change and anthropogenic insults. More frequent coral bleaching caused by global warming of seawater, severe storms and predation by crown-of-thorns starfish have degraded and diminished healthy reef ecosystems [2][3][4][5][6]. Since coral reef environments are constantly and dramatically changing, frequent, high-density coral monitoring is essential to assess these changes, in the hope of more effective coral reef preservation. ...
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Coral reefs have the highest biodiversity of all marine ecosystems in tropical and subtropical oceans. However, scleractinian corals, keystone organisms of reef productivity, are facing a crisis due to climate change and anthropogenic activities. A broad survey of reef-building corals is essential for worldwide reef preservation. To this end, direct observations made by coral-specialist divers might be supported by another robust method. We improved a recently devised environmental DNA (eDNA) metabarcoding method to identify more than 43 scleractinian genera by sampling 2 l of surface seawater above reefs. Together with direct observations by divers, we assessed the utility of eDNA at 63 locations spanning approximately 250 km near Okinawa Island. Slopes of these islands are populated by diverse coral genera, whereas shallow 'moats' sustain fewer and less varied coral taxa. Major genera recorded by divers included Acropora, Pocillopora, Porites and Montipora, the presence of which was confirmed by eDNA analyses. In addition, eDNA identified more genera than direct observations and documented the presence of previously unrecorded species. This scleractinian coral-specific eDNA method promises to be a powerful tool to survey coral reefs broadly, deeply and robustly.
... Tropical cyclones have accounted for most of the coral decline recorded in Australia's Great Barrier Reef (GBR) (De'ath et al., 2012), and the importance of storms may be even higher in the high-latitude reefs of Southern Japan, where the frequency and intensity of cyclones are increasing (Tu and Chou, 2013). A recent study showed that typhoons can cause shifts in coral morphology dominance (i.e., from foliose to bushy) in the upper mesophotic coral reefs from Okinawa (White et al., 2017). Storms and typhoons have been reported to be associated with increases and shifts in phytoplankton compositions and to influence the calcification of corals in Ishigaki reefs (Blanco et al., 2008;Sowa et al., 2014). ...
... More specific locality-based monitoring studies examining changes in benthic cover and compositions in the region has been on the increase, with recent studies done in Indonesia , Philippines , Singapore (Guest et al. 2016), Thailand , Vietnam Vo 2013), Hong Kong (Wong et al. 2018b), Japan (Hongo and Yamano 2013), and Taiwan (Keshavmurthy et al. 2019). As reefs continue to change in composition with each stressor, particularly bleaching events and typhoons, monitoring must accommodate and note these changes in the long term (Baird et al. 2005, Harii et al. 2014, White et al. 2017. With considerable monitoring requirements needed to cover the vast area in this region, greater participation, especially with citizen science and new local capacity, can expand the scope of studies and help provide more detailed insights into how reefs change over time (Lau et al. 2019, Obura et al. 2019, Gurney et al. 2019. ...
In summary for Southeast Asia: Philippines. Over the last decade, mean coral cover showed strong declining trends in the South Philippine Sea and the Sulu Sea, with marginal declines in the North Philippine Sea, Visayas Region (inland seas) and the Celebes Sea. Coral cover increased in the West Philippine Sea from 10% in 2008 to 32% in 2018. Overall, the cover data reported here are higher than a recent report by Licuanan et al. (2019), mainly because most of the sites surveyed here are located within marine protected areas. Between 2015 and 2017, coral bleaching was reported in 36 (54%) of the 66 coastal and island provinces surveyed. Most of the confirmed bleaching reports were in 2016 (79%), when bleaching incidences were reported almost year-round, although most reports (81%) were of low to mild bleaching. Moderate to severe coral bleaching was reported between April and October in 2016. The following year also saw bleaching, but reports were generally of low to mild bleaching.
... In recent years, China has carried out a number of coral reef restoration projects and practices along the coast of Hainan Island, Weizhou Island, and Dapeng Bay. Although these projects are distributed in the highly suitable areas predicted by our model, the restoration effect is not as good as expected because of poor water quality and extreme weather such as typhoons (Herbeck et al., 2011;Hongo et al., 2012;Li et al., 2013;White et al., 2017;Zheng et al., 2021b). We suggest that overall planning and actions for coral conservation networks be undertaken in the future to effectively mitigate coral vulnerability and enhance system resilience. ...
Scleractinian corals build the most complex and diverse ecosystems in the ocean with various ecosystem services, yet continue to be degraded by natural and anthropogenic stressors. Despite the rapid decline in scleractinian coral habitats in South China, they are among the least concerning in global coral vulnerability maps. This study developed a rapid assessment approach that combines vulnerability components and species distribution models to map coral vulnerability within a large region based on limited data. The approach contained three aspects including, exposure, habitat suitability, and coral-conservation-based adaptive capacity. The exposure assessment was based on seven indicators, and the habitat suitability was mapped using Maximum Entropy and Random Forest models. Vulnerability of scleractinian corals in South China was spatially evaluated using the approach developed here. The results showed that the average exposure of the study region was 0.62, indicating relatively high pressure. The highest exposure occurred from the east coast of the Leizhou Peninsula to the Pearl River Estuary. Aquaculture and shipping were the most common causes of exposure. Highly suitable habitats for scleractinian corals are concentrated between 18°N–22°N. Only 21.6 % of the potential coral habitats are included in marine protected areas, indicating that there may still be large conservation gaps for scleractinian corals in China. In total, 37.7 % of the potential coral habitats were highly vulnerable, with the highest vulnerability appearing in the Guangdong Province. This study presents the first attempt to map the vulnerability of scleractinian corals along the coast of South China. The proposed approach and findings provide an essential tool and information supporting the sustainable management and conservation of coral reef ecosystems, addressing an important gap on the world's coral reef vulnerability map.
... This is because environmental disturbances such as coral bleaching and storm damage generally attenuate relatively quickly with increasing depth (Bridge et al. 2014;Smith et al. 2014). In general, deeper habitats may not be impacted by disturbances to the same extent as shallow habitats (but see Bonagaerts et al. 2013;White et al. 2017), creating a more stable environment for some fishes, especially in the case of thermal anomalies (Brown 1997;Glynn 1996;Neal et al. 2014). Nevertheless, distinct assemblages of fishes inhabit mesophotic reef ecosystems (e.g. ...
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Coral reef fishes often exhibit specific or restricted depth distributions, but the factors (biotic or abiotic) that influence patterns of depth use are largely unknown. Given inherent biological gradients with depth (i.e. light, nutrients, habitat, temperature), it is expected that fishes may exploit certain depths within their environment to seek out more favourable conditions. This study used baited remote underwater video (BRUV) systems to document variation in the taxonomic and functional (trophic and size) structure of a fish assemblage along a shallow to upper-mesophotic depth gradient (13–71 m) at a submerged, offshore shoal in the northern Great Barrier Reef. BRUVs were deployed during two separate time periods (February and August 2017), to separately examine patterns of depth use. Both the relative abundance and diversity of reef fishes declined with depth, and there were pronounced differences in the taxonomic and functional structure of the fish assemblage across the depth gradient. In shallow habitats (< 30 m), the fish assemblage was dominated by herbivores, detritivores, planktivores and sessile invertivores, whereas the fish assemblage in deeper habitats (> 30 m) was dominated by piscivores and mobile invertivores. Depth and habitat type were also strong predictors for important fisheries species such as coral trout (Plectropomus spp.), emperors (Lethrinus spp.) and trevallies (Carangid spp.). We found limited evidence of temporal changes in depth and habitat use by fishes (including fisheries target species), although recorded temperatures were 4 °C higher in February 2017 compared to August 2017.
... fish, corals, sponges, algae) inhabiting these deeper meso photic coral ecosystems (MCEs) (~30− 150 m) would be protected and/or isolated from anthropogenic and naturally occurring stressors affecting shallow reefs, and might represent a viable refuge for genetically diverse sources of larvae in the future (see Bongaerts et al. 2010, Semmler et al. 2017). Unfortunately, research from different localities has shown that MCEs are prone to the same stressors and disturbances as their shallow-water counterparts, thus highlighting the importance of protecting these deeper reefs (Appeldoorn et al. 2016, White et al. 2017, Rocha et al. 2018. ...
Sponges are fundamental components of coral reef communities and, unfortunately, like other major benthic members, they too have been impacted by epizootic and panzootic events. We report on the prevalence of disease-like conditions affecting populations of the giant barrel sponge Xestospongia muta across shallow and mesophotic coral reefs off La Parguera Natural Reserve (LPNR) and Mona Island Marine Reserve (MIMR) in Puerto Rico. Four different conditions affecting X. muta were observed during our surveys, of which 3 have been previously reported: cyclic spotted bleaching (CSB; apparently non-lethal), Xestospongia-tissue wasting disease (X-TWD; apparently lethal), and sponge orange band disease (SOB; sparsely associated with X-TWD infected individuals). Additionally, we describe a fourth condition, Xestospongia-tissue hardening condition (X-THC), a previously unreported disease recently observed along the insular shelf margin off LPNR and MIMR. Within LPNR, a total of 764 specimens of X. muta were inspected and measured. Of these, 590 sponges (72.2%) had CSB, 25 (3.27%) had signs of X-TWD, 7 (0.92%) had SOB, and the remaining 142 (18.6%) were apparently healthy. Three colonies inhabiting upper mesophotic depths on the LPNR insular shelf showed signs of CSB and X-TWD. At MIMR, video-transect surveys revealed a total of 514 colonies, of which 40 (7.78%) had signs of CSB and/or X-TWD, 14 (2.72%) were affected by X-THC, while the remaining 460 (89.5%) showed no external signs of disease and appeared healthy. The presence of 4 concomitant disease-like conditions in barrel sponges of Puerto Rico is alarming, and indicative of the deteriorating status of Caribbean coral reefs.
... However, until now there has been no example of documented observations regarding Fungiidae movement and behavior from subtropical waters in the typhoon-prevalent western Pacific Ocean. Coral reef slopes in this region can be expected to be different from the previously investigated areas listed above as they are strongly affected by the large waves that are generated by typhoons (Hongo et al., 2012;White et al., 2013White et al., , 2017Harii et al., 2014). Thus, we expect that the mobility of mushroom corals in Okinawa may differ in characters from those seen in previous works. ...
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Offshore Onna Village, Okinawa Island, Japan, there is a large and densely covered coral assemblage of free-living mushroom corals (Scleractinia: Fungiidae) on a reef slope at depths from 20 m to 32 m, covering an area of approximately 350 × 40 m 2. From previous research, it is known that migration distances of mushroom corals may depend on coral shapes, coral sizes, substrate, and bottom inclination. However, until now there have been no published examples of regular Fungiidae movement and behavior from typhoon-exposed coastlines, such as those in the western Pacific Ocean. Our surveys across three years offshore Onna Village show that mushroom corals always move in down-slope direction from shallow to deeper reef zones. The results indicated that mushroom corals migrated faster in autumn than in other seasons, and that oval-elongate fungiids, and particularly those with a smooth underside, migrated more quickly than species with other shapes. Surprisingly, we observed a negative relationship between the presence of typhoons and migration rates. We also observed active migration by fungiid individuals to escape situations in which they were threatened to become overgrown by Acropora corals, or when they needed to escape from burial underneath coral debris.
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Disturbance is common in natural ecosystems, but increasingly defines them. While there are many descriptions for the dynamics of an ecosystem's response to disturbance, there are few descriptions for the dynamics of the disturbance itself. I describe a novel application of a model based on the production of amplitude envelopes in acoustics and electronic music synthesis, with varying parameters Attack, Decay, Sustain, and Release (ADSR). I show that varying the parameters of the ADSR model is sufficient to produce and vary the qualitative disturbance regimes described by previous authors, and is capable of producing dynamics not previously considered. I tested the utility of the ADSR model by applying it to a logistic growth model. I found that manipulating the attack and release parameters of the ADSR model changes the population dynamics estimated by these models. This implies that responses to disturbance are determined not only by the resilience and resistance of the ecological system, but also the dynamics of the disturbance itself. My hope is that the ADSR model will prove useful to researchers in either describing disturbances in long‐term ecological data, or in producing disturbances for simulations or experiments. In this idea paper, I propose that a tool commonly used in acoustics and electronic music synthesis, the envelope generator, may be useful for researchers wishing to describe or simulate ecological disturbances of varying temporal dynamics.
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Over the past few decades, extreme events -such as ocean warming, typhoons, and coral bleaching- have been increasing in intensity and frequency, threatening coral reefs from the physiological to ecosystem level. In the present study, the impacts of rising seawater temperatures, typhoons, and coral bleaching events on benthic communities were seasonally assessed over a 21 month-period, using photo-transects at 11 sites in Kenting National Park (KNP), Taiwan. Between August 2015 and April 2017, seven typhoon events were recorded and in situ seawater temperatures in KNP reached a maximum of 31.2 • C, as opposed to an average maximum SST of 28.8 • C (2007-2016). The state and response of benthic communities to these events were interpreted based on the environmental conditions of KNP. The repeated storms lowered the levels of thermal stress during the 2015-2016 El Niño event and may have mitigated its impact on the Taiwanese coral reefs. However, storm-induced local shifts from coral to macro-algae dominance were observed. Storms may mitigate the negative effects of heatwaves, but the mechanical damage induced by the storms may also decrease the structural complexity of reefs and their associated diversity. Eventually, despite reef persistence, the composition and function of remnant communities may profoundly diverge from those in regions with less active storms.
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Growth rates of the major Caribbean reef framework-building coral Orbicella spp. decrease with increasing water depth and light attenuation. However, reliable, spatially distributed growth rates for corals deeper than 30 m are rare, and the combined influence of coral framework accretion, secondary framework accretion, and framework macroboring on net framework calcification in these habitats is poorly constrained. To better understand the growth limits and spatial variability of Orbicella-dominated mesophotic coral reef ecosystems, live platy samples of Orbicella franksi were collected at 3 upper mesophotic reef habitats with varying structural characteristics on the Puerto Rican Shelf, south of St. Thomas, US Virgin Islands. Average mesophotic coral linear extension rates, determined by standard X-radiographic techniques and confirmed by stable isotopic analyses, were 0.80 ± 0.03 mm yr^−1 (±SE), slower than previously recorded for Orbicella spp. at shallower US Virgin Island reefs. However, coral cover at 2 of the mesophotic reefs was considerably higher than at nearby shallow-water St. Thomas reefs, implying that fast coral growth rates are not necessarily needed to maintain Caribbean reefs with high coral cover and structural complexity. A probable reason for this is reduced bioerosion with depth. Rates of net coral framework calcification were significantly different between the neighboring mesophotic coral reef habitats, likely a result of the complex interplay between site variability in irradiance, nutrient availability, and other factors. Analysis also indicated that the influence of El Niño−Southern Oscillation on water circulation and salinity as well as on water clarity and nutrient distribution in the Caribbean is reflected in the annual variability of mesophotic O. franksi growth rates. Site differences in net coral framework calcification suggest a potential long-term mechanism for the production or maintenance of heterogeneous reef-scale geomorphology along broad-sloping carbonate shelves colonized with mesophotic coral reef systems.
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Mesophotic coral ecosystems are extensive light-dependent habitats that typically form between 30 – 150 m depth in the tropical oceans. The forces that structure the benthic communities in these ecosystems are poorly understood but this is rapidly changing with technological advances in technical diving and remote observation that allow large-scale scientific investigation. Recent observations of southeastern Puerto Rican Shelf of the US Virgin Islands have shown that this Caribbean mesophotic coral ecosystem has distinct habitats within the same depth ranges and across small horizontal distances (<<1 km), that range from sparse hardbottom to vibrant coral reefs with stony coral cover >25%. High-resolution bathymetric mapping of the shelf edge revealed a topographically distinct semi-continuous 71 km-long relict barrier reef bank system. The purpose of this study was to characterize the pattern of mesophotic habitat development of the shelf edge and use this data to narrow the potential long-term and large-scale structuring forces of this mesophotic coral ecosystem. We hypothesized from limited preliminary observations that the shelf edge coral cover was limited in shallower portions of the bank and on the seaward orientation. Through stratified random surveys we found that increasing depth and decreasing wave driven benthic orbital velocities were positively related to coral abundance on the shelf edge. In addition, low coral cover habitats of the shelf edge contrasted strongly with adjacent on shelf banks surveyed previously in the same depth range, which had relatively high coral cover (>30%). Predictions of benthic orbital velocities during major storms suggested that mechanical disturbance combined with low rates of coral recovery as a possible mechanism structuring the patterns of coral cover, and these factors could be targets of future research.
Staghorn corals (genus Acropora) are the most obvious and important corals on coral reefs throughout the world, providing much of the beauty and variety seen on the reefs. This invaluable reference tool is the first major review of Acropora in over 100 years. It assesses all the known species worldwide, describing each in detail and illustrating the range of variability of form with habitat and geographic location. The classification, evolution and worldwide distribution of all species are reviewed and illustrated with colour plates, full page black and white plates and distribution maps. Details of the general biology of staghorn corals are discussed and illustrated.
Lobophylliidae is a family-level clade of corals within the ‘robust’ lineage of Scleractinia. It comprises species traditionally classified as Indo-Pacific ‘mussids’, ‘faviids’, and ‘pectiniids’. Following detailed revisions of the closely related families Merulinidae, Mussidae, Montastraeidae, and Diploastraeidae, this monograph focuses on the taxonomy of Lobophylliidae. Specifically, we studied 44 of a total of 54 living lobophylliid species from all 11 genera based on an integrative analysis of colony, corallite, and subcorallite morphology with molecular sequence data. By examining coral skeletal features at three distinct levels – macromorphology, micromorphology, and microstructure – we built a morphological matrix comprising 46 characters. Data were analysed via maximum parsimony and transformed onto a robust molecular phylogeny inferred using two nuclear (histone H3 and internal transcribed spacers) and one mitochondrial (cytochrome c oxidase subunit I) DNA loci. The results suggest that micromorphological characters exhibit the lowest level of homoplasy within Lobophylliidae. Molecular and morphological trees show that Symphyllia, Parascolymia, and Australomussa should be considered junior synonyms of Lobophyllia, whereas Lobophyllia pachysepta needs to be transferred to Acanthastrea. Our analyses also lend strong support to recent revisions of Acanthastrea, which has been reorganized into five separate genera (Lobophyllia, Acanthastrea, Homophyllia, Sclerophyllia, and Micromussa), and to the establishment of Australophyllia. Cynarina and the monotypic Moseleya remain unchanged, and there are insufficient data to redefine Oxypora, Echinophyllia, and Echinomorpha. Finally, all lobophylliid genera are diagnosed under the phylogenetic classification system proposed here, which will facilitate the placement of extinct taxa on the scleractinian tree of life.