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

Abstract

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.

Full text

Submitted 26 March 2017
Accepted 22 June 2017
Published 18 August 2017
Corresponding author
Kristine N. White, knwhite@ut.edu,
white.kristinen@gmail.com
Academic editor
Robert Toonen
Additional Information and
Declarations can be found on
page 10
DOI 10.7717/peerj.3573
Copyright
2017 White et al.
Distributed under
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OPEN ACCESS
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.
ABSTRACT
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
Management
Keywords Mesophotic, Succession, Coral reef, Pachyseris, Japan, Typhoon recovery, Shifting
communities
INTRODUCTION
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
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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
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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.
MATERIALS AND METHODS
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
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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,
2014).
RESULTS
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.
DISCUSSION
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
2012A
2012B
2014
2015
2012A
2012B
2014
2015
PachyserisPachyseris
Ec
h
inop
h
y
ll
i
a
Lithophyllon
Lithophyl
Ctenactis
Ct
ti
Galaxea
ea
Oxypora
Oxypora
Oxypora
Herpo
l
it
ha
Euphyllia
ll
Austra
l
omuss
a
Plerogyra P
a
v
o
n
a
G
oniastrea
D
ipsastraea
Lobophyllia
T
ridacnina
e
Merulinida
e
Stylophora
hora
Caula
stre
a
Astreo
p
or
a
Seriatopora
Unknown hard coral
co
Noncoral organism
s
Pectinia
Unknown
Montipora
ra
A
garaciida
e
Mycedium
i
Uk
Halomitr
a
Po
rite
s
Unknown Fungidae
nknown Fu
Merulina
u
Uk
Uk
k
Danafungia
anafungi
Pleuractis
r
ra
Ple
Pleu
Favites
vites
Acropora
A
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
0
5
10
15
0
10
20
30
0
10
20
0
5
10
15
20
0
25
50
75
100
0
5
10
15
0
10
20
30
0
10
20
30
40
20
Relative contribution (% morphology)
2012A 2012B 2014 2015
year
2012A 2012B 2014 2015
year
A
B*
E***
D
F
C* G
H
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.
ACKNOWLEDGEMENTS
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.
ADDITIONAL INFORMATION AND DECLARATIONS
Funding
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
planning.
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
paper.
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 http://dx.doi.org/10.7717/
peerj.3573#supplemental-information.
REFERENCES
Alvarez-Filip L, Dulvy NK, Côté IM, Watkinson AR, Gill JA. 2011. Coral identity
underpins architectural complexity on Caribbean reefs. Ecological Applications
21:2223–2231 DOI 10.1890/10-1563.1.
Alvarez-Filip L, Dulvy NK, Gill JA, Côté IM, Watkinson AR. 2009. Flattening of
Caribbean coral reefs: region-wide declines in architectural complexity. Pro-
ceedings of the Royal Society of London B: Biological Sciences 276:3019–3025
DOI 10.1098/rspb.2009.0339.
Baker EK, Puglise KA, Harris PT (eds.) 2016. Mesophotic coral ecosystems—a lifeboat for
coral reefs? Nairobi and Arendal: The United Nations Environment Programme and
GRID-Arendal, 98.
Beeden R, Maynard J, Puotinen M, Marshall P, Dryden J, Goldberg J, Williams G. 2015.
Impacts and recovery from severe Tropical Cyclone Yasi on the Great Barrier Reef.
PLOS ONE 10:e0121272 DOI 10.1371/journal.pone.0121272.
Bellwood DR, Hughes TP, Folke C, Nyström M. 2004. Confronting the coral reef crisis.
Nature 429:827–833 DOI 10.1038/nature02691.
Bongaerts P, Frade PR, Hay KB, Englebert N, Latijnhouwers KR, Bak RP, Vermeij
MJ, Hoegh-Guldberg O. 2015. Deep down on a Caribbean reef: lower mesophotic
depths harbor a specialized coral-endosymbiont community. Scientific Reports
5:7652 DOI 10.1038/srep07652.
Bongaerts P, Muir P, Bridge TCL. 2013. Cyclone damage at mesophotic depths on
Myrmidon Reef (GBR). Coral Reefs 32:935 DOI 10.1007/s00338-013-1052-y.
Bongaerts P, Ridgway T, Sampayo EM, Hoegh-Guldberg O. 2010. Assessing the
‘‘deep reef refugia’’ hypothesis: focus on Caribbean reefs. Coral Reefs 29:309–327
DOI 10.1007/s00338-009-0581-x.
Bruno JF. 2014. How do coral reefs recover? Science 345:879–880
DOI 10.1126/science.1258556.
White et al. (2017), PeerJ, DOI 10.7717/peerj.3573 11/15

Connell JH, Hughes TP, Wallace CC. 1997. A 30-year study of coral abundance, recruit-
ment, and disturbance at several scales in space and time. Ecological Monographs
67:461–488 DOI 10.1890/0012-9615(1997)067[0461:AYSOCA]2.0.CO;2.
Cowles HC. 1899. The ecological relations of the vegetation on the Sand Dunes of
Lake Michigan. Part I.-geographical relations of the Dune Floras. Botanical Gazette
27:95–117 DOI 10.1086/327796.
Darling ES, Alvarez-Filip L, Oliver TA, McClanahan TR, Côté IM. 2012. Evaluating
life-history strategies of reef corals from species traits. Ecology Letters 15:1378–1386
DOI 10.1111/j.1461-0248.2012.01861.x.
Davis GE. 1982. A century of natural change in coral distribution at the Dry Tortugas: a
comparison of reef maps from 1881 and 1976. Bulletin of Marine Science 32:608–623.
Denis V, Mezaki T, Tanaka K, Kuo C-Y, De Palmas S, Keshavmurthy S, Chen CA.
2013. Coverage, diversity, and functionality of a high-latitude coral community
(Tatsukushi, Shikoku Island, Japan). PLOS ONE 8:e54330
DOI 10.1371/journal.pone.0054330.
Dixon GB, Davies SW, Aglyamova GV, Meyer E, Bay LK, Matz MV. 2015. Genomic
determinants of coral heat tolerance across latitudes. Science 348:1460–1462
DOI 10.1126/science.1261224.
Dudgeon SR, Aronson RB, Bruno JF, Precht WF. 2010. Phase shifts and stable states on
coral reefs. Marine Ecology Progress Series 413:201–216 DOI 10.3354/meps08751.
Dustan P. 1975. Growth and form in the reef-building coral Montastrea annularis.
Marine Biology 33:101–107 DOI 10.1007/BF00390714.
Gardner TA, Cote IM, Gill JA, Grant A, Watkinson AR. 2005. Hurricanes and Caribbean
coral reefs: impacts, recovery patterns, and role in long-term decline. Ecology
86:174–184 DOI 10.1890/04-0141.
Gittenberger A, Reijnen BT, Hoeksema BW. 2011. A molecularly based phylogeny
reconstruction of mushroom corals (Scleractinia, Fungiidae) with taxonomic
consequences and evolutionary implications for life history traits. Contributions to
Zoology 80:107–132.
Graham NA, Chong-Seng KM, Huchery C, Januchowski-Hartley FA, Nash KL. 2014.
Coral reef community composition in the context of disturbance history on the
Great Barrier Reef, Australia. PLOS ONE 9:e101204
DOI 10.1371/journal.pone.0101204.
Graham NA, Jennings S, MacNeil MA, Mouillot D, Wilson SK. 2015. Predicting climate-
driven regime shifts versus rebound potential in coral reefs. Nature 518:94–97
DOI 10.1038/nature14140.
Halford A, Cheal AJ, Ryan D, Williams DM. 2004. Resilience to large-scale disturbance
in coral and fish assemblages on the Great Barrier Reef. Ecology 85:1892–1905
DOI 10.1890/03-4017.
Harmelin-Vivien M. 1994. The effects of storms and cyclones on coral reefs: a review.
Journal of Coastal Research 12:211–231.
Hoeksema BW. 1989. Taxonomy, phylogeny and biogeography of mushroom corals
(Scleractinia: Fungiidae). Zoologische Verhandelingen 254:1–295.
White et al. (2017), PeerJ, DOI 10.7717/peerj.3573 12/15

Hoeksema B, Cairns S. 2015. Scleractinia. In: Fautin DG, ed. Hexacorallians of the world.
World Register of Marine Species. Available at http:// www.marinespecies.org/ aphia.
php?p=taxdetails&id=1363 (accessed on 02 May 2017).
Huang D, Arrigoni R, Benzoni F, Fukami H, Knowlton N, Smith ND, Stolarski
J, Chou LM, Budd AF. 2016. Taxonomic classification of the reef coral family
Lobophylliidae (Cnidaria: Anthozoa: Scleractinia). Zoological Journal of the Linnean
Society 178:436–481 DOI 10.1111/zoj.12391.
Huang D, Benzoni F, Fukami H, Knowlton N, Smith ND, Budd AF. 2014. Taxonomic
classification of the reef coral families Merulinidae, Montastraeidae, and Diploas-
traeidae (Cnidaria: Anthozoa: Scleractinia). Zoological Journal of the Linnean Society
171:277–355 DOI 10.1111/zoj.12140.
Hughes TP. 1985. Life histories and population dynamics of early successional corals. In:
Proceedings of the fifth international coral reef congress, Tahiti, 4. 101–106.
Hughes TP. 1994. Catastrophes, phase shifts, and large-scale degradation of a Caribbean
coral reef. Science-AAAS-Weekly Paper Edition 265:1547–1551.
Hughes TP, Baird AH, Dinsdale EA, Moltschaniwskyj NA, Pratchett MS, Tanner JE,
Willis BL. 2012. Assembly rules of reef corals are flexible along a steep climatic
gradient. Current Biology 22:736–741 DOI 10.1016/j.cub.2012.02.068.
Hughes TP, Jackson JBC. 1985. Population dynamics and life histories of foliaceous
corals. Ecological Monographs 55:141–166 DOI 10.2307/1942555.
Kahng SE, Copus JM, Wagner D. 2014. Recent advances in the ecology of mesophotic
coral ecosystems (MCEs). Current Opinion in Environmental Sustainability 7:72–81
DOI 10.1016/j.cosust.2013.11.019.
Laliberté E, Legendre P. 2010. A distance-based framework for measuring functional
diversity from multiple traits. Ecology 91:299–305 DOI 10.1890/08-2244.1.
Laliberté E, Legendre P, Shipley B. 2014. FD: measuring functional diversity from
multiple traits, and other tools for functional ecology. R package version 1.0-12.
Available at https:// CRAN.R-project.org/ package=FD.
Lavorel S, Grigulis K, McIntyre S, Williams NSG, Garden D, Dorrough J, Berman S,
Quétier F, Thébault A, Bonis A. 2008. Assessing functional diversity in the field–
methodology matters! Functional Ecology 22:134–147
DOI 10.1111/j.1365-2435.2007.01339.x.
Leichter JJ, Genovese SJ. 2006. Intermittent upwelling and subsidized growth of the
scleractinian coral Madracis mirabilis on the deep fore-reef slope of Discovery Bay,
Jamaica. Marine Ecology Progress Series 316:95–103 DOI 10.3354/meps316095.
Lukoschek V, Cross P, Torda G, Zimmerman R, Willis BL. 2013. The importance of
coral larval recruitment for the recovery of reefs impacted by Cyclone Yasi in the
central Great Barrier Reef. PLOS ONE 8:e65363 DOI 10.1371/journal.pone.0065363.
McClanahan TR, Ateweberhan M, Graham NAJ, Wilson SK, Sebastian CR, Guillaume
MM, Bruggemann JH. 2007. Western Indian Ocean coral communities: bleaching
responses and susceptibility to extinction. Marine Ecology Progress Series 337:1–13
DOI 10.3354/meps337001.
White et al. (2017), PeerJ, DOI 10.7717/peerj.3573 13/15

Nozawa Y, Lin C-H, Chung A-C. 2013. Bathymetric variation in recruitment and relative
importance of pre- and post-settlement processes in coral assemblages at Lyudao
(Green Island), Taiwan. PLOS ONE 8:e81474 DOI 10.1371/journal.pone.0081474.
Ohara T, Fujii T, Kawamura I, Mizuyama M, Montenegro J, Shikiba H, White KN,
Reimer JD. 2013. First record of a mesophotic Pachyseris foliosa reef from Japan.
Marine Biodiversity 43:71–72 DOI 10.1007/s12526-012-0137-0.
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL,
Solymos P, Henry M, Stevens H, Wagner H. 2016. Vegan: community ecology
package. R package version 2.3-5. Available at https:// CRANR-project.org/ package=
vegan.
Pearson RG. 1981. Recovery and recolonization of coral reefs. Marine Ecology Progress
Series 4:105–122 DOI 10.3354/meps004105.
Perry CT, Smithers SG, Kench PS, Pears B. 2014. Impacts of Cyclone Yasi on nearshore,
terrigenous sediment-dominated reefs of the central Great Barrier Reef, Australia.
Geomorphology 222:92–105 DOI 10.1016/j.geomorph.2014.03.012.
Pillay RM. 2002. Field guide to corals of Mauritius. Albion: Albion Fisheries Research
Centre, Ministry of Fisheries, 334.
Platt WJ, Connell JH. 2003. Natural disturbances and directional replacement of species.
Ecological Monographs 73:507–522 DOI 10.1890/01-0552.
R Core Team. 2014. R: a language and environment for statistical computing. Vienna: R
Foundation for Statistical Computing. Available at http:// www.R-project.org/ .
Rachello-Dolmen PG, Cleary DFR. 2007. Relating coral species traits to environmental
conditions in the Jakarta Bay/Pulau Seribu reef system, Indonesia. Estuarine, Coastal
and Shelf Science 73:816–826 DOI 10.1016/j.ecss.2007.03.017.
Shinn EA. 1976. Coral reef recovery in Florida and the Persian Gulf. Environmental
Geology 1:241–254 DOI 10.1007/BF02407510.
Shinzato C, Mungpakdee S, Arakaki N, Satoh N. 2015. Genome-wide SNP analysis
explains coral diversity and recovery in the Ryukyu Archipelago. Scientific Reports
5:18211 DOI 10.1038/srep18211.
Smith TB, Brandtneris VW, Canals M, Brandt ME, Martens J, Brewer RS, Kadison E,
Kammann M, Keller J, Holstein DM. 2016. Potential structuring forces on a shelf
edge upper mesophotic coral ecosystem in the US Virgin Islands. Frontiers in Marine
Science 3:Article 115 DOI 10.3389/fmars.2016.00115.
Stoddart DR. 1974. Post-hurricane changes on the British Honduras reefs: re-survey of
1972. In: Cameron AM, Cambell BM, Cribb AB, Endean R, Jell JS, Jones OA, Mather
P, Talbot FH, eds. Proceedings of the Second International Symposium on Coral Reefs.
Vol. 2. Brisbane: Great Barrier Reef Committee, 473–483.
Veron JEN. 2000. Stafford-Smith M, ed. Corals of the world. Vol. 3. Cape Ferguson:
Australian Institute of Marine Science Monograph Series.
Wallace C. 1999. Staghorn corals of the world: a revision of the coral genus Acropora.
Collingwood: CSIRO, 421.
Weinstein DK, Klaus JS, Smith TB. 2015. Habitat heterogeneity reflected in mesophotic
reef sediments. Sedimentary Geology 329:177–187 DOI 10.1016/j.sedgeo.2015.07.003.
White et al. (2017), PeerJ, DOI 10.7717/peerj.3573 14/15

Weinstein DK, Sharifi A, Klaus JS, Smith TB, Giri SJ, Helmle KP. 2016. Coral
growth, bioerosion, and secondary accretion of living orbicellid corals from
mesophotic reefs in the US Virgin Islands. Marine Ecology Progress Series 559:45–63
DOI 10.3354/meps11883.
White KN, Ohara T, Fujii T, Kawamura I, Mizuyama M, Montenegro J, Shikiba H,
Naruse T, McClelland TY, Denis V, Reimer JD. 2013. Typhoon damage on a
shallow mesophotic reef in Okinawa, Japan. PeerJ 1:e151 DOI 10.7717/peerj.151.
White et al. (2017), PeerJ , DOI 10.7717/peerj.3573 15/15